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Saturday, 23 July 2016
The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees
Published Date , Volume 46, Issue 5,pp 813–839 Title The role of stored carbohydrates and nitrogen in the growth and stress tolerance of planted forest trees
Author
Pedro Villar-Salvador,
Mercedes Uscola,
Douglass F. Jacobs
Abstract Plants store compounds that supplement external resources to maintain primary functions. We reviewed the role of stored non-structural carbohydrates (NSC) and nitrogen (N) in juvenile woody species for spring growth and cold and drought stress tolerance, which are crucial processes for early performance of forest plantations. Plant functional types differed in NSC and N partitioning and allocation to new growth. In general, however, new leaves/shoots were more enriched in remobilized resources than new fine roots. Conifers used less remobilized resources than broadleaf species for fine root growth. New shoots/leaves were mostly comprised of remobilized N (>60 %) in conifers and broadleaf deciduous species, while broadleaf evergreens relied more on soil N (<50 % remobilized N). In contrast, few differences among functional groups existed in the contribution of remobilized carbon (C) to new leaves/shoots, which comprised 28–45 % of stored C reflecting the importance of current photosynthesis and distinctions in C and N remobilization physiology. The amount of N remobilized by an organ was positively related to its contribution to seedling N content. However, leaves are priority N sources in evergreens, which remobilized more N than predicted by their contribution to seedling N content. In contrast, roots in broadleaf evergreens and conifers were poor contributors of remobilized N. Under low stress, spring growth has little effect on NSC reserves. However, prolonged and intense photosynthesis depression strongly reduces NSC. In contrast, N reserves usually decline after planting and their replenishment takes longer than for NSC reserves. Strong storage reduction can hinder seedling stress acclimation and survival capacity. Resource storage can be promoted in the nursery by arresting plant growth and supplying resources at a higher rate than seedling growth and maintenance rate. We conclude that the way in which woody plants manage stored resources drives their growth and stress tolerance. However, plant functional types differ in storage physiology, which should be considered in silvicultural management. Introduction
Plants consume significant amount of nutrients and energy to maintain their main functions: growth, respiration, reproduction and defense. A large part of these resources is obtained from the soil and atmosphere. However, very often these sources do not meet plant demand because resources have been reduced by competition (Malik and Timmer 1996) or abiotic factors limit their availability in the environment such as extreme soil temperatures or drought (Millard and Grelet 2010). Moreover, main plant functions frequently occur simultaneously (for instance growth and reproduction or concomitantly growth of plant organs), imposing a strong resource demand that plants usually cannot meet by current uptake of external nutrients (Uscola et al. 2015). In these cases, plants rely on stored compounds, which are mobilized to supplement external resources and fulfill plant demand.
Storage can be defined as the process by which plants build up compounds that can be mobilized in the future from one organ to another to support main plant functions (Chapin III et al. 1990). Plant storage can be classified into three categories (Chapin III et al. 1990; Millard and Grelet 2010):
Accumulation, which is the increase in compounds that do not directly promote growth as a result of acquisition exceeding plant demand. This likely is the main storage component in seedlings when subjected to any cultivation practice that slows or stops growth but does not inhibit photosynthesis and nutrient uptake.
Reserve formation, which involves the metabolically regulated synthesis of storage compounds that might otherwise directly promote growth. Compounds can be stored throughout the plant or in particular plant compartments and mobilized to support future growth and functioning of other organs. Reserve formation potentially can compete for resources with other plant functions (Chapin III et al. 1990; Palacio et al. 2014).
When accumulated compounds or reserves are mobilized to support plant function and growth this physiological process is termed remobilization. The movement of remobilized compounds among tissues is termed translocation (Millard and Grelet 2010).
Recycling or resorption, when compounds that are currently involved in the functioning of a specific organ are withdrawn following breakdown of biochemical machinery and structural components in senescing organs. Resorption mainly affects mineral nutrients and only a small fraction of C is recycled from vegetative organs (Aerts and Chapin III 2000). On average, perennial plants recycle around 50 % of N and P from senescent leaves, with evergreen woody plants having lower resorption efficiency than deciduous species, although some differences exist among growth forms and plant functional types (Aerts 1996). Recycled nutrients are usually stored and remobilized later to sustain plant functions.
Stored “mobile” compounds are of varied nature. Quantitatively and according to their functional relevance, non structural carbon (mainly carbohydrates) (NSC) and nitrogen (N) are the most important stored compounds (Kozlowski 1992; Millard et al. 2007; Millard and Grelet 2010), but plants also store and mobilize significant amounts of mineral nutrients such as potassium, magnesium and phosphorus (Nambiar and Fife 1991; Proe et al. 2000). Most macronutrients can be remobilized but some mineral nutrients such as calcium, iron and heavy metals are not remobilized or recycled (Nambiar and Fife 1987; Chapin III et al. 1990).
Levels of stored compounds fluctuate under short-term (hours–days), as in many carbohydrates that vary on a daily time scale (Lambers et al. 2008), seasonal (weeks–month; Hoch et al. 2003; Körner 2003) and annual time frames (Vargas et al. 2009; Dietze et al. 2014). Part of the NSC and N plant pools can also remain immobilized in plant biomass and unavailable for metabolism (Millard et al. 2007; Vizoso et al. 2008). Consequently, “physiological or ecological depletion” of NSC and N does not necessarily mean that organs are completely devoid of these compounds.
The amount of stored resources and the way that plants manage them may have adaptive value under specific environmental scenarios. Differences in the amount of stored resources across species has been linked to recovery capacity after catastrophic loss of leaves or roots by disturbances (Cruz et al. 2003; Hoffmann et al. 2003; Palacio et al. 2007) and resisting prolonged stress conditions such as deep shade, low winter temperature and water stress (Canham et al. 1999; Poorter and Kitajima 2007; O’Brien et al. 2014). Differences in stored resources can also influence plant performance at an intra-species scale. For instance, the ability of Sabal palmetto seedlings to recover from aboveground tissue loss after grazing, burial or fire is related to differences in NSC content among individuals (McPherson and Williams 1998). Similarly, field survival and growth of planted seedlings in forest restoration projects has been positively related to tissue N and NSC levels both on a concentration and content basis (Marshall 1985; Puttonen 1986; van den Driessche 1991a; Ritchie and Landis 2010). Several physiological processes linked to NSC and N seedling status such as remobilization of stored compounds for new growth, metabolism maintenance and stress tolerance can drive seedling outplanting performance (Cuesta et al. 2010; McDowell 2011; Villar-Salvador et al. 2012).
Several reviews have thoroughly addressed the ecological and physiological relevance of NSC (Kozlowski 1992; Körner 2003; Millard et al. 2007; Dietze et al. 2014) and N (Millard 1996; Millard and Grelet 2010) storage in plants. Specifically to forestry applications, several studies have also analyzed the utility of NSC and N status as a seedling quality attribute and its utility for predicting seedling outplanting performance in forest plantation projects (Ritchie 1984; Marshall 1985; Mattsson 1997). van den Driessche (1991a) addressed how seedling N nutrition in conifers relates to outplanting performance and stress tolerance.
Here, we analyze the importance of stored NSC and N for seedling outplanting performance, focusing on two physiological processes linked to storage use by woody plant seedlings: new organ growth and tolerance to drought and frost stress. Specifically we carry out an extensive quantitative and qualitative review on the contribution of remobilized NSC and N for the construction of new organs in spring, which is crucial for seedling establishment and first year survival. We also review the differences in N and NSC distribution among seedlings of distinct functional types in woody plants. Finally, we review how nursery and post-nursery practices affect the NSC and N reserves of planted seedlings and identify gaps of knowledge on storage physiology that deserve future research.
Nature and distribution of NSC and N in seedlings of woody plants
Starch, sucrose, glucose and fructose make up >80 % of NSC in wet temperate trees (Hoch et al. 2003). Raffinose and stachyose are other common NSC in plants although at a much lower concentration than the former sugars. A variety of sugar alcohols, such as sorbitol and pinotol, can also be found in specific taxonomic groups but they are quantitatively less important than common NSC (Kozlowski 1992; Hoch et al. 2003).
N is stored as amino acids and specific vegetative proteins, which are formed in the bark after leaf senescence in the fall or during periods of high N uptake for seasonal demand such as in spring growth (Wetzel and Greenwood 1989; Binnie et al. 1994; Stepien et al. 1994; Lambers et al. 2008). N can also be stored as NO3 in fast-growing herb species supplied with high N-NO3 (Millard 1988). The inactive form of Rubisco can be considered a form of vegetative storage protein and its concentration can strongly increase upon N supply, explaining why N fertilization often does not increase photosynthesis rate in many plants (Valladares et al. 2000; Warren and Adams 2004; Millard et al. 2007). In temperate and cold climate woody plants, other “strictly speaking” vegetative storage proteins are formed in leaves and in the parenchyma cells of bark and wood in stems and roots; their levels strongly increase during the cold season and decrease during bud break (Wetzel and Greenwood 1989; Binnie et al. 1994; Stepien et al. 1994).
Seedlings and saplings of main functional types in woody plants have important differences in the partitioning of stored NSC and N during winter, with Quercus species (oaks) showing distinct partitioning patterns among broadleaf species (Table 1). Overall, broadleaf deciduous seedlings contain more N and NSC in roots than seedlings of broadleaf evergreens and conifers. Among broadleaf deciduous woody plants, Quercus species partitioned more stored resources to roots and less to stems than the non-Quercus species. Among evergreens, conifers were the functional type that partitioned more N to leaves, and they partitioned more N and NSC in leaves than in the rest of the organs. Broadleaf evergreen non-Quercusspecies partitioned N among main organs in a similar proportion, while broadleaf evergreen Quercus species partitioned around three more times N in roots and leaves than into stems. In relation to NSC, broadleaf evergreen non-Quercus species tended to contain more NSC in leaves than in stems and roots, which showed small differences in NSC partitioning. In contrast, around 70 % of NSC was partitioned to roots in broadleaf evergreen Quercusspecies.
Table 1
Partitioning (%) of N and NSC in different organs in young plants (seedlings and saplings) in different functional types of woody plants
Broadleaf deciduous
Broadleaf evergreens
Conifers
Non-Quercus
Quercus
Non-Quercus
Quercus
Nitrogen
(n = 16)
(n = 4)
(n = 8)
(n = 7)
(n = 6)
Leaves
0
0
37 ± 3.5
40 ± 3.8
55 ± 4.1
H = 35.6***
Stems
50 ± 4.1
24 ± 8.2
36 ± 5.8
15 ± 6.2
13 ± 6.7
H = 23.4***
Roots
50 ± 3.8
76 ± 7.7
31 ± 4.3
46 ± 5.8
32 ± 4.6
F = 8.9***
NSC
(n = 9)
(n = 3)
(n = 6–11)
(n = 6–7)
(n = 8–12)
Leaves
0
0
41 ± 4.6
17 ± 4.6
43 ± 4.0
F = 22.5***
Stems
39 ± 3.5
18 ± 6.1
30 ± 4.3
14 ± 4.3
26 ± 3.8
F = 5.77**
Roots
61 ± 4.2
82 ± 7.3
29 ± 3.8
72 ± 4.8
28 ± 3.7
F = 26.8***
Data are from plants sampled in fall or winter prior to field planting and are means ± 1 SE. Last column shows statistical results of ANOVA or Kruskal–Wallis tests. * P ≤ 0.05; ** P < 0.01; *** P ≤ 0.001; see Supplementary material for literature review details and reviewed studies. Numbers in brackets indicate the number of species reviewed in a specific group
Variation among functional groups in N and NSC partitioning mostly reflects differences in mass partitioning such as reported for winter C partitioning in seedlings of Mediterranean evergreen species (Uscola et al. 2015). For instance, Quercus species have large tap roots and consequently, relatively more reserves are allocated to coarse roots. However, some organs such as leaves in evergreens might act as priority storage sites, i.e. they contain more stored NSC or N than predicted from their size (Uscola et al. 2015). Specific adaptive traits can modify this general trend. Thus, root or stem resprouters generally allocate more C and N to the roots or stems, respectively, than do non-sprouting species (Palacio et al. 2007).
The contribution of stored NSC and N to new root and shoot growth
New root growth immediately after planting is crucial to hydrologically couple seedlings to the soil (Grossnickle 2005). Poor initial root growth can cause seedling water stress that hinders photosynthesis and growth, ultimately leading to damage or mortality. This and other physiological processes involved in seedling establishment were synthesized in Burdett’s plantation establishment model (Burdett 1990). In seasonally dry climates, such as the Mediterranean and Tropical climate, the main challenge for seedlings after establishment during the wet season is to survive the dry period. This is linked to the capacity of seedlings to avoid lethal water stress, which is mostly achieved by having a large, deep root system during the dry season (Grossnickle 2005; Padilla and Pugnaire 2007; Villar-Salvador et al. 2012). Because growth is very sensitive to reduction in plant water potential (Hsiao 1973), seedling root elongation will remain arrested during the dry period (Padilla and Pugnaire 2007) as long as the plant is under water stress. Consequently, seedlings need to produce a large and deep root system before the onset of the dry period. Furthermore, planted seedlings produce new shoots prior to the dry season, which usually enhances plant photosynthetic and competitive capacity (Cuesta et al. 2010).
Burdett (1990) suggested that current photosynthesis largely fuels root elongation during seedling establishment. This is the dominant paradigm mainly for conifers among forest managers and scientists (Luxmoore et al. 1995; Ritchie and Landis 2010). The paradigm stems from studies published in the 1970–1990s, which showed that photosynthesis reduction by shading, girdling or growing plants in CO2-depleted atmospheres depresses root growth in conifers (van den Driessche 1987; Philipson 1988; van Den Driessche 1991b; Noland et al. 1997). Similarly, 14C or 13C pulse labeling studies, which allow quantifying partitioning of labeled photosynthates throughout the plant also seemed to support this paradigm (Gordon and Larson 1968; Ursino et al. 1968). For instance, van den Driessche (1987) observed that the 14C recovered in new roots during the spring in 14C-fall labeled plants, was comparatively lower than the 14C recovered in seedlings that were labeled during active spring root growth. All these studies point out that current photosynthesis is intricately involved in new root growth of conifers but they do not indicate the magnitude of its contribution to final construction of new roots.
Stored NSC can also significantly contribute to new organ growth, independently if the plant remains photosynthetically active. For instance, in two broadleaf evergreen trees and one evergreen conifer, stored C made up >65 % of total C in new fine roots during early spring (Uscola et al. 2015). However, for deciduous trees in which new roots resume elongation before budburst (Riedacker 1976), initial new root and shoot growth relies completely on stored NSC (Dyckmans and Flessa 2002; Vizoso et al. 2008).
Other stored resources along with NSC must be considered to control root and shoot growth during seedling establishment and the subsequent rapid growth phase in spring. Thus, in the evergreen conifer Pinus sylvestris, remobilization of N, K and Mg supplied 83, 82 and 52 %, respectively of new shoot growth demand of these nutrients (Proe et al. 2000). Similarly, remobilized N contributed to early root growth in four evergreen species more than current uptake of soil N (Uscola et al. 2015).
We quantitatively reviewed published studies (see Supplementary material for methodological details of the review and consulted studies) to assess if main functional types of woody plants (conifers, and broadleaves both evergreens and deciduous) differ in the use of stored NSC and N to the construction of new shoots and roots. Regarding N, the contribution of storage to new shoot growth decreased through time in conifers and deciduous broadleaf species, while it increased among evergreen broadleaf species (Fig. 1). New shoots/leaves were mostly made of remobilized N in conifers and deciduous broadleaf species (>65 %, 1 and 2 months after bud break) with small differences between both functional types. The proportion of remobilized N in new shoots/leaves of evergreen broadleaves was significantly lower (<50 %) than in conifers and broadleaf deciduous species 1 and 2 months after budburst. Regarding C, we did not detect any effect of time after budburst on the composition of organs in remobilized C. The proportion of remobilized C in new leaves/shoots was on average lower than 50 % in all functional types, without significant differences among them (Fig. 1). The low dependence on remobilized C for new shoot/leaves in broadleaf deciduous woody plants may provide an erroneous perspective of the storage physiology of these plants as most data in the database were taken when foliage was nearly or completely unfolded. Deciduous trees can allocate high amounts of currently fixed C to new organ growth after reaching autotrophy, which usually occurs rapidly after budburst and significantly before new leaves are completely mature (Keel and Schädel 2010). However, during budburst and in the very early shoot growth stages, deciduous plants mainly use stored C to support leaf/shoot growth (Dyckmans and Flessa 2002).
Fig. 1
Contribution of remobilized N (a) and C (b) to new shoot/leaf growth in juveniles of main functional types of woody plants. Data are means ± 1 SE. As the contribution of remobilized N was influenced by the time after bud break (see text), a least square means estimated at three moments after bud break. b The contribution of remobilized C after most leaves had completely unfolded and matured. Inserted numbers are the number of species studied in each functional type. See Supplementary material for methodological details of the review
In conifers, contribution of stored N and C to the construction of new fine roots was low while in deciduous woody plants the contribution of remobilized N was high (Table 2). The proportion of remobilized N in new fine roots of broadleaf evergreens was low and similar to values in conifers. Conversely, remobilized C in new roots of broadleaf evergreen species was higher than in conifers and similar to values in broadleaf deciduous species. Notably, the limited data on conifer new fine roots (Pinus nigra and Pinus halepensis; Maillard et al. 2004; Uscola et al. 2015) seem to support the idea that conifers strongly rely on current photosynthesis and soil N for early new root growth. We found very few studies reporting the contribution of C and N reserves to new (fine) root growth, which probably precluded finding significant differences among plant functional types (Table 2). Therefore, results should be taken with caution. The low number of species in our data base was because most of these studies did not distinguish between fine and coarse roots. Both types of roots should be considered separately because they have distinct sink strength for remobilized resources (Uscola et al. 2015) and varying patterns of nutrient uptake (Hawkins et al. 2014).
Table 2
Contribution (%) of remobilized N and C to the growth of new fine roots in three main functional types of woody plants
Broadleaf
Conifer
Evergreens
Deciduous
Remobilized N
20 ± 5
(n = 4)
66 ± 26
(n = 3)
15 ± 4
(n = 2)
Remobilized C
39 ± 6
(n = 4)
38 ± 32
(n = 2)
15 ± 3
(n = 2)
Data are means ± 1 SE and values in brackets are the number of studied species in each group. Species included in the analysis are: Quercus coccifera, Q. ilex, Q. suber, Olea europaea (broadleaf evergreens); Malus domestica, Fagus sylvatica and Q. robur(broadleaf deciduous); P. halepensis and P. nigra (conifers)
Our quantitative review indicates that new fine roots tend to depend more on external sources for their construction in spring while new leaves/shoots tend to be constructed using more remobilized resources than external resources, especially for N (>50 %) (Fig. 1; Table 2). This might be explained because new leaf/shoot growth is a stronger N and NSC sink than new root growth (Grelet et al. 2001; Uscola et al. 2015), which likely results in external resource uptake not meeting resource demand for new leaf/shoot growth. Differences in the contribution of remobilized resources in the construction of new roots and new leaves/shoots has important implications for seedling cultivation, highlighting the importance of N- and NSC-loading seedlings for fueling shoot growth after seedling establishment.
Dependence of new root growth on stored C in broadleaf deciduous woody plants will presumably depend on whether root elongation resumption is before or after foliage development. When shoot growth occurs before new fine root elongation due to low soil temperature, new root growth can be supported by C supplied by new foliage. Similarly, when soil N take up does not meet plant N demand due to either low soil temperature or low N availability, new growth strongly relies on remobilized N (Millard and Proe 1993; Millard et al. 2001; Silla and Escudero 2003).
The role of plant organs as suppliers of remobilized resources differed among woody plants. In (evergreen) conifers, most of the N remobilized to support new organ growth of juveniles is derived from foliage (Table 3). Consequently, stems and roots in conifers seem to be poor sources of remobilized N. Conversely, stems and roots supplied 50 % of remobilized N in broadleaf evergreens. Finally, stems contributed slightly more N to remobilization than roots in broadleaf deciduous woody plants. Interestingly, we observed that the contribution of an organ to N remobilization is directly related to the contribution of the organ to the seedling’s initial N content (Fig. 2). However, leaves in evergreens (both broadleaf and conifers), and stems to a lesser extent, proportionally “donate” more remobilized N than predicted by their contribution to seedling N content. In contrast, roots donate less N than predicted by their contribution to seedling stored N. This is implicated by the fact that most foliage and stem data in Fig. 2 have a proportion of remobilized N relative to their contribution in seedling N content >1 (i.e., data are above the line that represents equal proportion of remobilized N and contribution in seedling N content), while this proportion is <1 for most root data. Two causations may help to explain this trend. First, it is possible that seedlings follow a resource conservation strategy and may only have a greater use of the N stored in roots when recovery after disturbances or other stress factor that require a surplus of N. Second, the proportion of soluble N (mobile N) might differ among organs types (Vizoso et al. 2008).
Table 3
Relative contribution (%) of different organs to remobilized N for seedling/sapling spring growth in three main functional types of woody plants
Broadleaf evergreens (n = 5)
Broadleaf deciduous (n = 8)
Conifers (n = 4)
Foliage
48 ± 5
0
78 ± 6
F = 55.7***
Stems
30 ± 4
54 ± 3
7 ± 5
F = 32.8***
Roots
22 ± 6
46 ± 5
15 ± 7
F = 8.4**
Data are means ± 1 SE. See Supplementary material for methodological details of the review and used references. ** P < 0.01
Fig. 2
Relationship between the relative contribution of an organ to total remobilized N in a plant and the relative contribution of the organ to plant content. Data are from 17 species and for each species, we show data for foliage, stems and roots, except for deciduous plants, which lacked leaves as data were obtained from dormant seedlings. The dotted line indicates the 1:1 relationship between both variables. Black symbols are data of evergreens while white symbols are the data of deciduous woody species. Dots, inverted triangles and squares are data for leaves, stems and roots, respectively. We show the values for a representative conifer (Pn, Pinus nigra), broadleaf evergreen shrub (Q, Quercus coccifera) and a broadleaf deciduous tree (Qr, Quercus robur)
Data on the contribution of plant organs to remobilized C during new shoot and root growth in spring at a whole plant scale are scarce. In three Mediterranean broadleaf evergreen trees, Uscola et al. (2015) found that old leaves (45–59 %) and coarse roots (25–34 %) were the main contributors of remobilized + respired C during spring growth. In the Mediterranean pine, P. halepensis, needles supplied around 73 % of lost C during spring growth (Uscola et al. 2015). In contrast, P. nigra foliage had a minor role and roots supplied 75 % of lost C (Maillard et al. 2004). Finally, in the seedlings of the deciduous tree Quercus robur, stems and coarse roots contributed 46 and 54 % to the C remobilized and respired for spring growth (Vizoso et al. 2008).
Remobilization of stored NSC and N for spring growth usually reduces their concentration over the short term. However, reduction of N reserves often is greater than NSC reserves (Millard and Grelet 2010), which recover faster than N reserves after spring growth (Bazot et al. 2013). Seedling establishment seems to have a low impact on seedling stored NSC. In three out of five Mediterranean trees species, NSC concentration in 1-year-old seedlings had a clear increase in NSC relative to pre-planting NSC values when seedlings were outplanted under full sun conditions for 26 days (Fig. 3). In the oak Q. ilex, NSC had no variation while NSC significantly decreased relative to pre-planting NSC values in Q. coccifera. Under moderate stress conditions (i.e., 65 % reduction in photosynthetic photon flux density), NSC pools were little affected in all species except for Q. coccifera, which showed a strong reduction. Thus, under non-limiting or moderate stress field conditions current photosynthesis usually replenishes seedling NSC pools rapidly during the establishment phase. Finally, only when current photosynthesis was suppressed by shoot darkening, NSC pools strongly declined in all species, but primarily in the two fast growing pines. Shoot growth in spring has a greater impact on seedling stored resources than new root growth during the establishment phase because it is a stronger resource sink than early new root growth (Uscola et al. 2015). In 1-year-old Q. robur seedlings, woody compartments (the main sources of remobilized N and C) had a net loss of N after spring shoot growth and new N uptake could not replenish initial storage levels on the short term. In contrast, C content of woody compartments recovered in the same period to the pregrowth levels as a result of currently assimilated C (Fig. 3). Thus, contrary to N, plants rarely are C-limited in most growth conditions and C storage is maintained even when subjected to a short growing season (Hoch and Körner 2003) or to repeated cutting or grazing (McPherson and Williams 1998; Palacio et al. 2008, 2011).
Fig. 3
a Variation in the content of old C (left subfigure) and old N (right subfigure) in woody organs (coarse roots and stems) of 1-year old Q. robur seedlings before bud break and after leaf growth completion in spring. The white bar shows the C incorporated due to current photosynthesis or N taken up from the soil (redrawn from data in Vizoso et al. 2008). b Relative variation in seedling NSC concentration relative to pre-planting seedling NSC concentration in 1-year old seedlings of five Mediterranean woody species, which were planted in the field in March for 26 days. n = 4. Seedlings were planted under three light conditions: full sun, shade (photosynthetic flux density was reduced by 65 %) and complete darkness. Shade was achieved by enclosing the shoots within an insect screen while darkness was achieved by enclosing the shoots inside a polystyrene box wrapped with aluminum foil. All seedlings grown under sun and shade conditions produced significant amounts of new roots (Villar-Salvador, unpublished data). In both figures data are means ± 1 SE
Factors affecting resource mobilization
As with other functional attributes, mobilization of stored resources shows plasticity and varies depending on environmental and plant endogenous factors. Most published literature on the environmental factors affecting mobilization of stored compounds has been performed with N, while mobilization of NSC has received little attention. As shown in the previous section, the use of remobilized compounds for new growth varies among plant functional types and across the growing season (Fig. 1), among years (Silla and Escudero 2003) and changes through ontogeny (Gilson et al. 2014). Uscola et al. (2015) also found that the importance of remobilized N and C for new shoot growth increased with relative growth rate among evergreen woody plants. In the following section we review other factors that are relevant for seedling outplanting performance and that can affect the way plants use stored resources.
Plant N content
Nitrogen remobilization is mainly a source-driven process, i.e., the greater the amount of stored N, the higher N remobilization is, which increases growth capacity (Millard 1996; Millard and Grelet 2010). This, in part, explains why high N content plants have superior growth and are more competitive after transplanting in the field than are low N plants (van den Driessche 1991a; Cuesta et al. 2010; Villar-Salvador et al. 2013b; Oliet et al. 2013). Conversely, NSC remobilization is a sink strength driven process and consequently the amount of remobilized NSC does not depend on the size of NSC storage (Millard and Grelet 2010).
Demonstrating that increasing N remobilization enhances new growth is not an easy task. Remobilization experiments frequently have confounding effects that complicate the ability to identify specific factors that control plant growth. For instance, nursery N fertilization increases seedling N content (see “Nursery cultivation practices affecting seedling NSC and N storage” section) and bud development (Islam et al. 2009) and these plants can have higher outplanting growth (Villar-Salvador et al. 2013a). To ascribe this superior growth to remobilization may be erroneous because an increase in plant N content often co-varies with photosynthetic capacity in N fertilization experiments: high N fertilized seedlings have greater foliage with a higher photosynthetic rate than do low N fertilized plants (Oliet et al. 2013), which can also drive outplanting growth (Guehl et al. 1989). We designed a study to control for these confounding effects and to assess if differences in N remobilization are related to growth differences. We produced two phenotypes of P. halepensis seedlings, which had the same size with no differences in morphology but differed strongly in their N content (Table 4). This was achieved by using a fall fertilization regime where half of the plants were supplied with a high N fertilization rate under cool temperature conditions, which prevented plants from growing but did not completely hinder N uptake capacity. The remaining plants were not fertilized during the fall. Seedlings were transplanted to a plot in early winter and subjected to strong weed competition in spring. Further cultivation and field measurement details can be consulted in the legend of Table 4 and in Cuesta et al. (2010). Both types of seedlings did not differ in photosynthesis rate in the nursery before transplanting. However, spring photosynthesis rate measured under field conditions was significantly lower in the fall N-loaded plants than in the unfertilized plants. At the end of the spring, shoot growth was 60 % higher in N-loaded plants than in seedlings that were not fertilized in the fall. Concomitantly, N remobilization was 3.5 times higher in fall N loaded plants than in unfertilized N seedlings, while soil N uptake did not differ among seedling types. These results supports the idea that greater remobilization due to higher N content enhances field growth.
Table 4
Nursery functional attributes and outplanting performance differences between fall N-loaded and unfertilized P. halepensis seedlings
Unfertilized seedlings
Fall N-loaded seedlings
P
At the end of cultivation
Plant mass (g)
2.30 ± 0.18
1.91 ± 0.20
0.22
Shoot N concentration (mg g−1)
11.2 ± 0.3
26.8 ± 0.8
<0.001
Plant N content (mg)
22 ± 2
27 ± 0.8
<0.001
Photosynthesis rate (μmol m−2 s−1)
2.31 ± 0.75
2.51 ± 0.74
0.84
Field performance in spring
Photosynthesis rate (μmol m−2 s−1)
0.90 ± 0.14
0.28 ± 0.16
0.02
Uptake from soil N (mg)
3.9 ± 2.6
2.5 ± 2.5
0.67
N remobilization (mg)
3.8 ± 2.0
13.5 ± 1.6
0.007
Stem volume growth (ml)
0.17 ± 0.02
0.28 ± 0.02
<0.001
Unfertilized seedlings were fertilized during the spring and summer of the first growing season in the nursery but did not receive any fertilization during the fall. Then plants were transplanted to a plot in early winter and experienced very high weed competition in spring of the second growing season. Nitrogen remobilization and uptake, and field net photosynthesis rate were measured at the end of the spring in five plants per treatment. Remobilization and uptake were determined on the same plants used for gas exchange measurements using a budget approach. Plant field growth was measured in late spring in 12–15 plants per treatment as the stem volume increase, which was calculated from the height and diameter of the stem assuming a cone shape. Cultivation and further experimental details can be consulted in Cuesta et al. (2010)
Soil fertility
Performance on poor soils can be increased if planted seedlings have high nutrient use efficiency. It has long been suggested that this could be attained if plants have high resorption efficiency and mainly rely on stored resources for new growth, which would reduce dependence on soil nutrients (Chapin III 1980; Salifu and Timmer 2003a). However, evidences indicate that N remobilization seems to be unaffected or little by soil fertility across plant functional types (Millard and Neilsen 1989; Millard and Proe 1991; Proe et al. 2000; Grelet et al. 2001; Cheng and Fuchigami 2002; Salifu and Timmer 2003a). Similarly, Aerts (1996) reviewed resorption efficiency studies covering 60 woody species and concluded that 63 % of the species showed no response to soil fertility while 32 % of the species showed a decrease in N resorption efficiency.
Competition and herbivory
Planted seedlings often are predated to varying degrees and have to compete with established vegetation. At a within-species scale, stored resources can play a significant role in overcoming browsing, disease and competition (McPherson and Williams 1998; Cruz et al. 2003; Cuesta et al. 2010). Stored C rather than current photosynthesis provided most of the C used for the construction of reaction tissues in P. sylvestris infected with a pathogenic fungus (Guérard et al. 2007).
Competition hinders growth and thus future competition capacity of plants by reducing the amount of stored resources. In Betula pubescens, competition resulted in smaller seedlings with less ability to store and, consequently, to remobilize N in the next growing season (Millet et al. 2005). However, competition did not hinder current N remobilization, but it reduced N uptake in P. halepensis. Consequently, remobilized N was the main source for new spring growth in seedlings competing with weeds, while soil N was the main N source in seedlings growing without weeds (Cuesta et al. 2010).
Damage of shoots frequently results in compensatory growth by increasing photosynthesis of undisturbed leaves and mobilization of stored resources in intact organs (Canadell and Lopez-Soria 1998; Oyarzabal and Oesterheld 2009). However, as for competition, herbivory may also reduce future remobilization capacity after a portion of stored resources are removed by predators (Millet et al. 2005). This explains in part why removal of the old leaves before bud burst in Q. ilex reduced N concentration in new leaves grown in spring (Cherbuy et al. 2001). The capacity of plants to use stored resources to recover after predation depends on the main storage sites. Among woody species, leaf predation may have a greater impact on evergreen species than in deciduous species because leaves are the main N storage sites in evergreens while woody organs are the main N storage sites in deciduous species (Millard et al. 2001). Accordingly, it can be hypothesized that conifers should be more vulnerable to leaf predation than broadleaf evergreen species (Table 3).
Water stress and shade
Few studies have analyzed the effect of water stress or shade on remobilization. As for competition, drought stress or shading in the current growing season may hinder remobilization capacity in the next growing season if it decreases seedling N and NSC content. Reduction in light to 20 % reduced starch content 50 % in Vitis vinifera roots, which are main sites of remobilized resources for spring growth. Consequently, leaf and roots were smaller in the next growing season compared with non-shaded vines (McArtney and Ferree 1999).
In contrast to remobilization, the effect of drought on foliage nutrient resorption has been studied more thoroughly. Premature and non-programmed leaf abscission in response to water stress may result in low nutrient resorption (del Arco et al. 1991; Harvey and van den Driessche 1999) with potential consequences for N storage and future remobilization. However, drought-induced leaf abscission will have little effect on N storage and growth the following year, provided that N uptake can occur during the cold season (Wendler and Millard 1996).
The role of NSC and N reserves in seedling drought and frost resistance
Plants seldom are C-limited but seedlings can be subjected to conditions between the nursery and the plantation site that significantly reduce seedling NSC and, consequently, may jeopardize out-planting performance. For instance, seedlings stored in darkness in refrigerated systems may have lower outplanting performance if not adequately hardened or stored for extended periods of time (Grossnickle and South 2014). Poor field performance of cold stored plants has been attributed in part to strong reduction in NSC levels (Ritchie 1982, Table 5). However, few studies have found a close relationship between field performance and seedling NSC following storage (Puttonen 1986; Cannell et al. 1990; Omi et al. 1994). Similarly, seedlings exposed to prolonged drought stress either after spring shoot growth or when planted under deep shade, such as in the understory of forest stands, might also show severe reductions in tissue NSC levels (O’Brien et al. 2014).
Table 5
Summary of the most frequently effects (increase ↑, decrease ↓ or no effect =) of main nursery practices on the concentration of N and NSC reserves
Nursery practices
Effect on N reserves
Effect on NSC reserves
References
Concentrat.
Content
Concentrat.
Content
Fertilization
Conventional/exponential fertilizationa
↑
↑
↓
= or ↓
van den Driessche (1992); Sanz-Pérez et al. (2007); Villar-Salvador et al. (2013b); Oliet et al. (2013); Heredia et al. (2014)
Fall fertilization
↑
↑
↑ ?
↑ ?
Islam et al. (2009); Oliet et al. (2011); Li et al. (2012); Andivia et al. (2014)
Foliar fertilization
↑
↑
↓ ?
↓ ?
Montville et al. (1996); Uscola et al. (2014a); Wuyts et al. (2015)
Hardening
Irrigation: moderate water stress for short periods
↑
↑ or =
↑ or =
↑ or =
Timmer and Miller (1991); van den Driessche (1992); Stewart and Lieffers (1993); Villar-Salvador et al. (1999); Villar-Salvador et al. (2013a); Sanz-Pérez et al. (2007); Sanz-Pérez et al. (2009)
↓ Photoperiod
↑ or =
↑ or =
↑ or =
↓ or =
Grossnickle et al. (1991); Tan (2007); Landhäusser et al. (2012b)
↓ Light intensity
↓
↓
↓
↓
Valladares et al. (2000); Villar-Salvador et al. (2004a); Baber et al. (2014)
Effects with question marks show hypothesized trends as no study on the effect of such nursery practice has been found
a In the conventional and exponential fertilization regime, nutrients are supplied at a constant and exponential rate, respectively through spring until the end of summer. In the fall fertilization regime nutrient supply continues or is increased through the fall
The capacity of planted seedlings to withstand frost and drought is related to tissue NSC concentration, mainly of soluble sugars (Sakai and Larcher 1987; Morin et al. 2007). Perennial plants from temperate and boreal biomes become increasingly frost tolerant through the fall and winter (Sakai and Larcher 1987; Mollá et al. 2006). This concomitantly occurs in parallel to an increase in tissue soluble sugars concentration (Ögren et al. 1997; Heredia et al. 2014). Starch hydrolysis provides a significant part of soluble sugars during cold hardening, which stabilizes cell membranes against cell dehydration caused by the freeze of extracellular water (Levitt 1980; Uemura and Steponkus 2003). Premature reduction in cold hardiness due to higher NSC respiratory consumption has been reported during spells of mild winter temperatures (Ögren et al. 1997). Galvez et al. (2013) observed that prolonged drought stress in the previous growing season enhanced winter mortality in two Populus species. This was attributed to low frost tolerance of root system linked to reduced root NSC. Similarly, Q. ilex seedlings cultivated in a mild winter nursery had 32 % less soluble sugar concentration and higher shoot dieback after heavy frosts in the field than seedlings cultivated in a cold winter nursery (Mollá et al. 2006).
The relationship between frost hardiness and seedling N storage is less straightforward than with NSC. There is general agreement that low tissue N concentration usually hinders cold acclimation (van den Driessche 1991a; Taulavuori et al. 2014). However, moderate to high tissue N concentration has been shown to increase (Andivia et al. 2012), reduce (Harvey and van den Driessche 1997) or have no effect on frost resistance (Thomas and Ahlers 1999). Taulavuori et al. (2014) reviewed 50 studies published since 1990–2014 and found that in 40 % of cases high N supply increased frost hardiness, while in 29 % of cases N had no effect. They concluded that plant frost hardiness generally increases when N increases within the optimal range for a given species. High tissue N concentration can increase frost tolerance by increasing NSC, as a result of enhanced photosynthesis, and the concentration of proteins involved in frost tolerance (Sheppard 1994; Duman and Wisniewski 2014). However, high tissue N concentration can also hinder frost hardiness if it delays shoot elongation cessation in the fall (Heredia et al. 2014).
As per cold tolerance, poor performance under dry conditions at an intraspecific level has also been linked to lower plant NSC. McDowell et al. (2008) proposed C starvation to be an important driver of tree mortality under dry conditions and several studies have provided indirect support for this idea. For instance, a large decrease in tissue NSC concentration at planting due to prolonged storage in refrigerated systems increased mortality and reduced growth after planting in P. sylvestris seedlings (Fig. 4). The relation was not linear, indicating that deterioration of plant performance does not occur until a critical NSC threshold is achieved. Similarly, dieback in P. sylvestris adults after prolonged and intense drought in NE Spain was greater in individuals that had the lowest NSC concentration (Galiano et al. 2011). Prolonged and intense drought reduced root and needle starch concentration in P. nigra seedlings, with mortality increasing rapidly when plants reached very low tissue starch levels (Guehl et al. 1993). However, these experiments provide circumstantial evidence regarding the role of NSC on plant mortality. Demonstrating that low stored NSC is a cause of plant mortality is a very difficult task due to many confounding effects. Recent experiments that were designed to specifically unravel the role of NSC on plant survival, have provided solid evidences that low NSC can jeopardize the capacity of plants to survive under dry conditions (Mitchell et al. 2013; Hartmann et al. 2013; O’Brien et al. 2014). For instance, by experimentally manipulating light conditions, O’Brien et al. (2014) produced seedlings with contrasting NSC concentration in 10 Borneo tree species without differences in morphology. After transplanting under drought conditions they observed that NSC enriched seedlings had delayed mortality and maintained higher water potential and NSC levels than low NSC seedlings.
Fig. 4
Relation of field mortality (black dots) and shoot growth (white dots) after one growing season with the needle glucose concentration at planting in P. sylvestris seedlings that were subjected to different storage regimes prior planting (adapted from Puttonen 1986)
NSCs are involved in osmotic adjustment, embolism and oxidative stress repair and defense, which are crucial physiological processes for plants to survive drought (Chaves et al. 2003; Salleo et al. 2004; Sevanto et al. 2014). Therefore, strong reduction in NSC can constrain the capacity of plants to meet NSC demand for these physiological processes and for maintenance metabolism (McDowell 2011). Moreover, water stressed plants have limited capacity to translocate stored NSC due to phloem failure, limiting NSC transport to where needed (Hartmann et al. 2013; Sevanto et al. 2014).
The importance of low NSC as a cause of seedling mortality depends on the strategy of plants to resist drought (McDowell et al. 2008; Mitchell et al. 2013). Drought avoiders or isohydric species, which close stomata at high tissue water potential, are prone to mortality through NSC-based processes as they potentially can be exposed to sustained periods of negative carbon balance. In contrast, drought tolerant or anisohydric species are able to maintain gas-exchange capacity at low water potential values, which prevents significant NSC reductions during dry periods. For anisohidric plants hydraulic failure caused by xylem embolism seems to be the main cause of death (McDowell et al. 2008; Mitchell et al. 2013).
Low seedling survival under dry conditions has also been related to low tissue N concentration (van den Driessche 1988; Oliet et al. 2013). Higher tissue N can support higher root and shoot growth as discussed in “Factors affecting resource mobilization” section. This is important for seedling establishment and vigorous root growth before the onset of the dry season, which is crucial for maintaining water uptake capacity during the dry season and gas-exchange capacity (Villar-Salvador et al. 2012).
Nursery cultivation practices affecting seedling NSC and N storage
Seedling quality is strongly influenced by nursery cultivation practices such as irrigation, fertilization, hardening, cold storage, and lifting/store or handling (van den Driessche 1991b; McKay 1997; Wilson and Jacobs 2006; Islam et al. 2009; Grossnickle 2012; Grossnickle and South 2014). These manipulations may result in changes in seedling size, root/shoot biomass allocation, cold hardiness, dormancy development, stress tolerance and storage reserves that affect subsequent seedling outplanting performance (Grossnickle 2012). Specifically, understanding how seedlings use stored resources to support growth is of practical importance for cultivating seedlings. Nursery practices should promote NSC and N storage in those species that strongly depend on these stored reserves for new growth. This can be accomplished by optimizing fertilization systems. Similarly, nurseries should promote traits conferring high C assimilation and soil N acquisition in species that primarily use external C and N sources to support new growth. This can be achieved by producing seedlings with high leaf area, photosynthetic rate, and large root systems. Photosynthetic rates can usually be enhanced by increasing foliar N concentration through an optimized fertilization regime.
Storage of NSC and N can be quantified using two components that although related, have different consequences for plant function. Compound “concentration” is relevant for osmotic- and mass flow rate-based physiological processes such as osmotic adjustment and cell membrane stability, cold hardiness and gas-exchange (Chaves et al. 2003; Villar-Salvador et al. 2004b; Warren and Adams 2004; Morin et al. 2007), while compound “content” better explains remobilization and absolute growth, persistence under sustained negative C balance situations or disturbance recovery (Poorter and Kitajima 2007; Millard and Grelet 2010; McPherson and Williams 1998). Thus, if two plants of the same species have the same N and NSC concentration but differing content of these compounds (for instance because one is larger than the other) and stored compounds are equally partitioned, both plants would likely have the same frost tolerance and photosynthetic rate but the plant with higher N and NSC content will have greater remobilization, growth capacity, and potential to persist under deep shade conditions. A summary of the primary nursery cultivation practices and their effects on seedling NSC and N concentration and content is shown in Table 5. While culture is generally designed to minimize resource limitations and promote seedling growth, applying some level of stress to slow growth (and its corresponding demand for nutrients and current photosynthates) or supplying resources at higher rate than seedling growth rate may cause plants to re-allocate these resources toward reserves (Chapin III et al. 1990; Grossnickle et al. 1991; Landhäusser et al. 2012a). The final effect on NSC and N seedling content will depend on the balance between growth and concentration of these compounds.
Four aspects of fertilization can be modified to change seedling nutritional status: dosage, form of application, timing of application and N form applied. Dosage: N-based fertilizers (e.g., urea or ammonium nitrate) generally increase N concentration and content although the magnitude of response is species-specific and dependent on fertilizer application method (Birge et al. 2006; Villar-Salvador et al. 2013b). Conventional fertilization practices in bareroot and container seedling nurseries are often based upon providing seedlings with a constant fertilizer supply throughout the growing season using a moderate fertilizer supply (Landis et al. 1989). While use of this method usually achieves seedling morphology targets, there is a tendency for decline in foliar nutrient concentration due to growth dilution as the season progresses, which suggests nutrient stress due to excess fertilization at the beginning of the growing period and possible under-fertilization at the end of culture (Timmer 1997). Increasing the amount of nutrients applied can enhance formation of reserves but can extend the growing period and decrease the hardening of the seedlings, and thus reduce the cold resistance of the seedlings (Islam et al. 2009; Andivia et al. 2012). Effects of fertilization methods on NSC are less well studied though results generally suggest that fertilization decreases NSC concentration (Sanz-Pérez et al. 2007; Villar-Salvador et al. 2013a). Because fertilization also stimulates growth the final effect on plant NSC content will depend on the balance between NSC concentration and plant mass.
Form of application: While fertilization is generally targeted to root systems by application to soil or media, foliar fertilization represents an alternative application method to increase N reserves (Montville et al. 1996; Uscola et al. 2014a; Wuyts et al. 2015), especially if applied in late summer and in the fall.
Modifying the time of application can help rectify some of the disadvantages of increasing nutrient dosage. In this sense, exponential fertilization tailors fertilizer inputs to plant demand, generally involving low fertilization at the beginning of culture and high fertilization during the final stages of cultivation (Timmer and Aidelbaum 1996; Timmer 1997). This allows for luxury nutrient consumption, with optimal fertilization being that which maximizes N content without inducing toxicity (Salifu and Timmer 2003b; Salifu and Jacobs 2006; Birge et al. 2006) and produces N-loaded seedlings. Late season (fall) fertilization is a variant of N loading whereby conventionally grown seedlings are fertilized at relatively high rates after bud set in fall (van den Driessche 1985; Islam et al. 2009; Oliet et al. 2011; Andivia et al. 2014), which contrasts with traditional hardening practices that imply little to no fertilization during this period (Landis et al. 1989). However, even though this fertilization technique can enhance N concentration and content, the effect on NSC is not well known. For instance, Heredia et al. (2014) did not find leaf soluble carbohydrate concentration differences among conventional, exponential and fall fertilization in Q. ilex.
Finally, N form used in the fertilization program has a strong impact on physio-morphological attributes of seedlings. NH4+ fertilization tends to hinder plant growth, especially of fine roots, increasing plant N concentration, however it can reduce concentrations of other cations in plants and cause toxicity when applied at high rates (Britto and Kronzucker 2002; Uscola et al. 2014b). In contrast to NH4+, NO3− can be commonly supplied at higher concentrations without harmful effects on plants but easily stimulates growth even later in the growing season by diluting the N concentration of the seedlings (Landis et al. 1989; Cruz et al. 1993). Some nurseries alter the primary N form in the fertilizer depending on the season, using mainly NO3− during the spring and NH4+ in late season to stop growth and increase N concentration of the seedlings (Landis et al. 1989).
Irrigation intensity is usually adjusted according to growth phase and plant needs, with inputs gradually increasing during the growing period and a withholding of watering at the end of culture to help induce hardening (Landis et al. 1989). Reduced irrigation throughout the duration of culture results in lower plant biomass and less reserves (Timmer and Miller 1991). However, moderate stress applied for short periods during the hardening phase usually increases N and increases or has no effect on NSC concentration, but intense and prolonged drought stress act to decrease NSC concentration (Guehl et al. 1993; Stewart and Lieffers 1993; McDowell 2011; Villar-Salvador et al. 2004b, 2013a), eventually leading to mortality. The threshold balance between positive and negative effects of drought hardening on seedling development and its relation to N or NSC reserves are largely unstudied and provide opportunity for future research (Villar-Salvador et al. 2004b, 2013a). Evidence suggests that there may also be interactive effects of drought hardening and fertilizer application method, as Timmer and Miller (1991) reported increased N concentration in roots under dry conditions for exponential versus conventional fertilization and the opposite effect under a moist irrigation regime.
Other cultural practices that influence N and NSC reserves include shading, which generally decreases both compounds when applied for extended duration through the growing season (Valladares et al. 2000; Villar-Salvador et al. 2004a; Baber et al. 2014). Photoperiod manipulation (i.e., blackout or short-day treatment) involves reduction of photoperiod for several weeks during mid-summer and is often applied to species in boreal zones as a means to slow shoot growth and induce hardening. While researchers have emphasized dormancy and cold hardiness responses, evidence suggests that this practice may result in an increase or essentially no effect on N or NSC concentration (Grossnickle et al. 1991; Tan 2007; Landhäusser et al. 2012b). Cultivation density (bareroot and container) or container volumealso influence reserves, with generally an increase or no effect on N concentration and content as density decreases or container volume increases (van den Driessche 1984; Robbins and Pharr 1988; Aphalo and Rikala 2003; Dominguez-Lerena et al. 2006; Oliet et al. 2012; Dumroese et al. 2013); effects on NSC are less well documented, though a general trend of increasing seedling dry mass as density decreases or as container volume increases suggests that NSC reserves would increase concomitantly. Winter storage conditions may also affect N or NSC reserves. In Mediterranean environments, seedlings are generally stored outdoors until being transported for planting; exposure to lower fall and winter temperatures may result in accumulation of greater N and NSC reserves than that in warmer sites for the same genetic source (Mollá et al. 2006; Heredia et al. 2014). In temperate and boreal environments, seedlings are often stored in coolers (above or below freezing); prolonged cold storage acts to decrease NSC reserves (Ritchie 1982; Puttonen 1986; Cannell et al. 1990). Finally, poor handling practices can have a profound negative effect on NSC reserves; for example, Insley and Buckley (1985) reported that losses of lateral roots of broadleaved seedlings during plant handling might account for 20–40 % of total root carbohydrates.
Future Research Direction
Many studies have addressed the role of N remobilization on plant growth (see Supplementary material). However, most of these studies have been performed with temperate and boreal trees. Little information exists on species of other biomes and other functional types of woody plants, such as shrubs and chamaephytes (but see Palacio et al. 2014; Uscola et al. 2015). The need for studies on the use of NSC reserves for new growth is even more peremptory than stored N as we cannot presently elucidate clear use patterns of remobilized NSC among woody plants. Moreover, most studies have been performed on single species and studies have been made under different growth conditions, making conclusions on the adaptive meaning of stored resources use patterns difficult. Therefore, we need more comparative studies performed under the same environmental conditions (see Millard et al. 2001; Uscola et al. 2015).
Most studies showing a relation between plant survival, growth and disturbance recovery and NSC levels provide circumstantial evidence of the role of stored NSC in plant performance. Several confounding effects make it difficult to experimentally demonstrate the role of NSC on drought and cold survival. For instance, NSC content has been related to disturbance recovery of plants. However, it is possible that other resources such as N and P may co-vary with NSC and be as relevant as NSC for plant recovery (Moreira et al. 2012). Therefore, a major challenge of future research is designing experiments to address the specific role of major stored resources and their interactions.
Nitrogen nutrition affects the frost tolerance of plants but there is no clear consensus as to whether moderate to high N supply during the cold acclimation period increases frost tolerance in plants. The varying effects of nutrition on plant cold and drought tolerance might be due to differences among studies in whether seedlings were evaluated during active growth or in dormancy, species-specific differences and due to interactions with several environmental factors such as temperature during the cold acclimation phase. Therefore for late season fertilization be an effective seedling N-loading option, future research should assess which species are most suitable for this fertilization procedure and the optimum period during fall when it could be applied without negative effects on cold hardening.
Finally, there are several cultivation practices for which their effect on concentration and content of NSC are unknown such as fall and foliar fertilization, cultivation density and container volume.
Conclusions
Juveniles across functional types of woody plants show important differences in how they store and manage N and NSC reserves for spring growth and stress tolerance. Overall, broadleaf deciduous seedlings accumulate more N and NSC in roots than do broadleaf evergreens and conifers. Quercus species both deciduous and evergreens partitioned more stored resources to roots than the non-Quercus species. Among evergreens, conifers showed the highest N partitioning to leaves. In general, woody plants tended to use more remobilized resources for the construction of new leaves/shoots than for the new fine roots protruding out of the root plug after planting. However, conifers used less remobilized resources than broadleaf species for new fine root growth. Spring new shoot/leaf growth was mostly made of remobilized N (>60 %) in conifers and broadleaf deciduous species, while broadleaf evergreens relied more on soil N. In contrast, the contribution of remobilized C to new leaves/shoots showed few differences among functional types and comprised 28–45 % of organ C. This highlights the importance of current photosynthesis for new leaf/shoot growth and the differences between C and N remobilization physiology. The organs that supplied more remobilized N to support growth had higher contribution to seedling N content. However, leaves in evergreens seem to supply more remobilized N than predicted by their contribution to seedling N content, while roots showed the reverse pattern. Under non-limiting conditions, NSC storage is little affected after spring growth as current photosynthesis rapidly replenishes NSC storage. However, when seedling photosynthesis is depressed for long periods such as in cool storage, or due to intense and sustained drought stress or deep shade, NSC reserves can be significantly reduced, which potentially can impair outplanting performance. In contrast, N reserves usually are significantly reduced after seedling establishment or during early spring growth and their replenishment takes longer than NSC storage. Cultivation practices that apply some level of stress to slow growth of seedlings and supply resources at a higher rate than that of seedling growth rate can promote resource storage.
Acknowledgements
This research was supported by funds of Projects AGL2011-24296 (ECOLPIN) and CGL2014-53308-P (SERAVI) of the Spanish Ministry of Science and Innovation, Remedinal 3 (S2013/MAE-2719), of the Community of Madrid, and CCG2014/BIO-004 of the University of Alcalá.
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