Báo cáo lâm nghiệp: "Carbon and nitrogen allocation in trees"

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allocation in trees Carbon and nitrogen R.E. Dickson USDA-Forest Service, NCFES, Rhinelander, WI, U.S.A. compared to agronomic crops, we have Introduction only limited knowledge of carbon and interactions and for any growth nitrogen species in natural ecosystems. Although Growth of trees and all plants depends up- there have been many studies on compo- positive carbon balance maintaining on a nent biomass, nutrient content, and net despite continually changing environmen- primary production, the results are difficult tal stresses. Under natural conditions, to interpret and generally do not provide growth is commonly limited by several information on changes over time in environmental stresses operating at the varying environments. The primary reason same time. Thus, growth is the summation for interpretation problems is the lack of of a plant’s response to multiple environ- ’standard’ carbon allocation data sets mental stresses (Chapin et aL, 1987; developed for trees grown under ’opti- Osmond et al., 1987). Light, carbon, water mum’ conditions to compare with carbon and nitrogen are fundamental factors most allocation patterns found in stress situa- to limit growth. On a world-wide likely tions. A major objective of tree research basis, water availability is probably the should be to develop such ’standard’ data major factor limiting plant growth (Schulze sets on a few key or indicator species. et al., 1987). However, in many temperate Then carbon and nitrogen allocation pat- and tropical forests, nitrogen availability is terns found in trees under stress can be the most critical limiting factor (Agren, interpreted, and changes in allocation can 1985a). Thus, information provided by stu- be predicted for other species and other dies of carbon and nitrogen metabolism stress situations. and their interactions is necessary to understand plant growth. In this paper,I plan to review the current There has been an enormous amount of literature on carbon and nitrogen alloca- research on carbon and nitrogen interac- tion (the movement of carbon within the tions and plant growth, primarily with agri- plant) in trees. Because of space limita- cultural plants and primarily directed tions and other recent reviews on the towards harvestable plant parts. However, regulation of carbon partitioning (carbon
flow among different chemical fractions Smith and P;aul, 1988). Additional com- over time) at the cellular level (Champigny, plexities and differences arise between 1985; Huber, 1986; Geiger, 1987), parti- deciduous and evergreen trees. Deci- will not be addressed. Even after tioning duous and evergreen trees use different many years of research, we still know little strategies to maximize carbon gain and about the processes involved and the fac- utilization of both internal and external tors that regulate carbon and nitrogen allo- 1982). Deciduous resources (Schulze, cation in trees. Quantitative information on trees rapidly renew all of their leaves in basic allocation patterns and how these the spring at a relatively low carbon cost patterns change during the season is per unit leaf area but at a high cost of available for only a few annual plants of stored carbohydrate. Deciduous leaves No agronomic importance (Pate, 1983). are also very productive per unit leaf area, such detailed quantitative information on and much of the carbon fixed after leaf de- carbon and nitrogen allocation is available velopment is available for growth of stems for any tree species. However, there is and roots or for storage. In contrast, car- considerable descriptive information for bon costs of evergreen leaves are relative- carbon allocation in Populus (Isebrands ly high (Pearcy et al., 1987). However, and Nelson, 1983; Dickson, 1986; Bonicel only a small portion of total leaf mass et al., 1987), and for carbon and nitrogen is renewed each year. Carbon fixation allocation in fruit trees (Titus and Kang, continues in older leaves and overall 1982; Tromp, 1983; Kato, 1986). carbon gain may be similar to rapidly growing deciduous trees (Matyssek, All plants allocate carbon to maximize 1986). Although patterns of carbon fixa- competitive fitness, reproduction, and tion, partitioning to different chemical frac- growth within their various plant communi- tions, allocation within the plant and ties. Plants in different environments have cycling within the plant may differ between different ’strategies’ for allocation depend- and among deciduous and evergreen ing upon their life-forms (Schulze, 1982). trees in many details, the major seasonal Annual crop plants with basically four sea- patterns of carbon and nitrogen allocation sonal growth phases - early vegetative, are very similar. flowering, seed fill, and senescence - have been the subject of most studies on carbon and nitrogen allocation. These life- forms are relatively simple and there is Carbon allocation in trees much economic incentive to understand their basic biological mechanisms in order to manipulate growth and yield. In compar- Crop scientists have long recognized that ison, trees, which may live from 50 to carbon allocation is a major determinant of more than 5000 years, are much more dif- growth and yield (Gifford et aL, 1984) and ficult experimental subjects. During their have organized research programs ac- lives, trees go through several different cordingly. Understanding ’standard’ car- growth stages: seedlings, saplings, pole- bon allocation patterns in trees would stage, mature flowering and fruiting, and provide the background information ne- Each stage is characterized cessary for interpreting how these patterns senescence. by increasingly complex change with stiress and would provide the morpholo- crown gy and allocation patterns. In addition, knowledge necessary to develop physiolo- seasonal growth phases also alter alloca- gically based management strategies and tion patterns (Dickson and Nelson, 1982; genetic improvement programs.
the base. Basal leaflets may translocate Leaf development and carbon transport both to developing distal leaflets and out of the leaf (Larson and Dickson, 1986). development and physiological Structural However, not all compound leaves devel- processes change continuously from leaf op in this manner. In tomato (Lycopersi- initiation to full maturity. These changes con esculentum L.), terminal leaflets ma- not uniform throughout the lamina but are ture first and leaf development is from tip progress from tip to base in most plants. to base (Ho and Shaw, 1977). Northern The onset of translocation from a particu- red oak (Quercus rubra L.) has a simple lar lamina region is the best indicator of leaf with yet another developmental pat- tissue maturity. Translocation begins after tern. Red oak leaf and stem growth is epi- the sieve element-companion cell complex sodic with one or several flushes of growth matures and a translocatable product is each growing season. Within a flush, all produced in the tissue (Dickson and the leaves of that flush expand and ma- Shive, 1982). The simple leaf of cotton- ture at about the same time, although wood (Populus deltoides Bartr. Marsh.) there is an acropetal developmental gra- provides a good example of this develop- dient within the flush. Northern red oak mental pattern. Both anatomical and !4C transport studies show that leaf maturity leaves become autotrophic (they no long- er import photosynthate from older leaves) begins at the lamina tip and progresses at about 50% of full expansion. Transport basipetally. In contrast to cottonwood, the of photosynthate out of the leaf begins at compound leaves of green ash (Fraxinus the lamina base at about 50-60% of full pennsylvanica Marsh.) and honeylocust leaf expansion and from the whole leaf at (Gleditsia triacanfhos L.) mature first at
about 70-80% of full leaf expansion 3 leaf zones, approximately the top 5 (Dick- unpublished results). leaves (LPI 0--5) would be expanding and son, importing photosynthate, the middle 5 leaves (LPI 6-10) would be transporting Carbon transport patterns in deciduous both acropetally and basipetally in varying trees degrees, and the bottom 5 leaves (LPI 11-15) would be transporting primarily to larger lower stem and roots (Fig. 1in studies with !4C have shown that Labeling plants (e.g., with 45 leaves), essentially transport from source leaves to sink the same divisions hold except there are leaves is controlled by both the vascular more leaves (about 15) in each leaf zone. connections between source and sink and These same developmental and transport relative sink demand (Vogelmann et al., patterns would be found in all trees with 1982). For example, a source leaf on a indeterminate growth. 16-leaf cottonwood plant has vascular connections to sink leaves inserted 3 and 5 positions above the source leaf (Table I). Thus, a high percentage of photosynthate 1 - is transported to those sink leaves. In contrast, leaves inserted 1 and 4 positions above the source have no direct vascular connections to the source leaf and receive little !4C. The influence of sink strength is also illustrated in Table I by the percent !4C incorporated into the third leaf above the source leaf (e.g., leaves at leaf plasto- chron index (LPI) 4 and 5 above source leaves LPI 7 and 8). As a sink leaf ex- pands, more C0 is fixed in situ, and the 2 demand (sink strength) for imported pho- tosynthate decreases. By LPI 5 (source leaf 8), the entire lamina is approaching maturity and imports little 14 Photosyn- C. thate exported by LPI 8 is then available for younger leaves nearer the apex and for transport to lower stem and roots. Mature leaves below the source leaf nor- mally do not import photosynthate directly from distal source leaves but may import carbon (e.g., amino acids) that has cycted through the root system (Dickson, 1979). Leaf and transport development pat- terns within small trees are also fairly consistent. In 16-leaf cottonwood plants, the transition from upward to downward transport takes place quickly because of the small number of leaves on the plant (Fig. 1Ifaa 16-leaf plant were divided into
ported to the main stem and moves pri- lateral branches are also Developing sinks for carbon and nitrogen. Assi- marily downward to lower stem and roots. strong However, photosynthate from uppermost milate for early development of proleptic branches may be translocated acropetally branches (branches that develop from in the main stem and used in development dormant buds on older shoots) comes of the current terminal (Rangnekar et aL, from stem storage in deciduous trees and from both storage and current photosyn- 1969; Dickson, 1986). thate in evergreen trees. Photosynthate Within-plant carbon allocation patterns for early development of sylleptic bran- strongly influenced by sink strength of ches (branches that develop from current are developing leaves. The transport of car- year buds) is supplied primarily by the bon within northern red oak seedlings is a axillant leaf (Fisher et aL, 1983). Branch good example of this phenomenon. During sink strength decreases as more foliage a flushing episode (e.g., 2 leaf linear, Fig. leaves are produced. In cottonwood, syl- 2) more than 90% of the !4C translocated leptic branches become photosynthetically leaves was directed from first flush independent of the main plant after 10-15 5 upward developing second flush leaves to mature leaves have developed (Dickson, and stem, while about 5% was found in 1986). Photosynthate produced by indivi- lower stem and roots. During the lag dual leaves on a branch is distributed phase, when second flush leaves were within that branch in the same pattern as fully expanded, only about 5% of the !4C that described above for the main shoot of exported from first flush leaves was trans- a seedling or current terminal of a larger located upward, while 95% was translo- tree. Photosynthate not required for cated downward to lower stem and roots. branch growth and maintenance is trans-
First flush leaves responded again during the carbon fixed before budbreak is stored the third flush of growth with upward trans- in leaves, and some is translocated to location of 14 even though the mature C, lower stem and roots (Table II). Numerous !4C allocation studies have shown that leaves of the second flush were also translocating upward. Such shifts in the during the spring flush of growth both cur- direction of translocated photosynthate is rently fixed and stored carbohydrates are probably a major contributing factor to the translocated to new growth (Gordon and out-of-phase periodicity of shoot and root Larson, 1968; Schier, 1970; Webb, 1977; growth commonly observed in trees (Hoff- Smith and Paul, 1988). After new foliage man and Lyr, 1973; Drew and Ledig, 1980; begins to transport photosynthate, carbon is again allocat:ed to lower stem and roots. Sleigh ef al., 1984). This alternating pattern of upward trans- port to strong leaf sinks and downward transport after new leaf maturation in Carbon transport patterns in conifers and single flush conifers, such as red pine other evergreen trees (Pinus resinosa), is similar to that found in single flush deciduous trees (except the carbon for new leaf development in deci- Seasonal allocation patterns of newly duous trees comes initially from stem and fixed carbon in conifers is similar to those root storage pools). In conifers with mul- found in deciduous trees, but with impor- tiple flushes during the growing season, tant differences. Because leaves are acropetal and basipetal transport would already present, conifers may fix carbon also be cyclic - first to strong developing during warm early spring periods. Some of
back, general progressive decline and leaf sinks, then to lower stem and roots after full leaf expansion - just as in mul- eventual death. tiple flushing red oak (Fig. 2). Allocation of carbon to storage is a rela- low priority function. With bud-set tively Carbon allocation to storage and maturation of leaves in late summer and fall, leaf sink strength decreases and assimilate is translocated to lower stem Carbohydrate storage exhibits both diurnal and roots. This assimilate is preferentially and seasonal patterns. Diurnal patterns of used for xylem development or root carbon allocation were recently examined growth and then for storage. The timing in detail (Dickson, 1987). In addition, the and degree of change in direction of trans- seasonal variation in concentration and port strongly depend upon the phenology location of various storage compounds of the particular clone or tree species (Ise- has been examined in many tree species brands and Nelson, 1983; Nelson and lse- (Kramer and Kozlowski, 1979; Glerum, brands, 1983; Michael et al., 1988). In 1980; McLaughlin et aL, 1980; Nelson and addition, xylem growth and/or storage Dickson, 1981; Bonicel et al., 1987). takes place at different times in different Therefore in this review,I will only exam- parts of a tree depending upon growth of ine the interactions of tree growth and car- the particular organ. Cambial activity and bohydrate storage. xylem growth generally progress as a In perennial plants, wave from developing buds and branches, photosyn- excess thate is stored as carbohydrates, lipids to stem, to roots (Denne and Atkinson, and other chemical compounds. Storage 1987). Thus, diameter growth of larger of reserves is particularly important for roots takes place much later in the grow- plants growing in areas with large season- ing season than stems. Starch may be al climatic changes. Reserves are used for stored in root tissue early in the summer respiration and plant maintenance during before diameter growth starts (Wargo, the dormant season and for new growth in 1979). This starch is not hydrolyzed and spring. Stored products are also used for used for diameter growth, but remains in episodic growth flushes during the growing the ray and xylem parenchyma. This phe- season (Sleigh et al., 1984). Late season- nomenon indicates that current photosyn- al defoliation or repeated defoliation of thate is used for diameter growth and not deciduous trees may deplete reserves and stored assimilate. New fine root growth lead to branch die-back or death of the may also depend upon current photosyn- whole tree (Heichel and Turner, 1984). thate (van den Driessche, 1987; Philip- More importantly for tree growth and survi- son, 1988). Stored assimilates are used val, defoliation may initiate a cycle in for new leaf and shoot growth in the spring which many stress factors are involved. and for regrowth of leaves after defoliation For example, low carbohydrate reserves in (Gregory and Wargo, 1986; Gregory et stems and roots increase susceptibility to al., 1986). However, the degree to which cold winter temperatures, decrease foliage current photosynthate or stored assimilate regrowth, decrease root growth, increase can be used for stem or root growth water stress and susceptibility to summer requires much more research with !4C drought and increase susceptibility to root tracers to determine the distribution of cur- rots and other pathogens (Wargo and rent photosynthate between active growth Montgomery, 1983; Gregory et al., 1986). and storage pools in different tissues (Gle- Such multiple stresses may cause top die- 1980). rum,
Nitrogen allocation in trees mediated release of organically bound nitrogen and its conversion into ammo- nium and nitrate. Movement in the opposi- major environmental factor limiting The te direction converts inorganic nitrogen growth in many temperate forests is into organic forms and results in immobili- nitrogen availability. Many experiments zation. Net mineralization will occur only conducted under controlled conditions when the nitrogen released by decomposi- have shown that plant growth is directly tion exceeds that required by the microflo- related to the internal nitrogen concentra- ra (Carlyle, 1986). This occurs when the tion up to some optimum concentration substrate C:N ratio decreases to that of (Agren, 1985b; Ingestad and Lund, 1986; the microbial biomass; thus the C:N ratio Ingestad and Agren, 1988). Thus, if nitro- at which mineralization begins can be gen supply decreases, internal nitrogen associated with site and other factors concentration decreases and growth rate (Berg and Ekbohm, 1983). In high C:N lit- decreases. In addition, as the amount of ter, essentially all nitrogen is immobilized functional biomass increases, the amount by microorganisms and is not available to of nitrogen required per unit time higher plants. However, mycorrhizal asso- increases and the amount of nitrogen sup- ciations may increase the ability of higher plied must also increase or growth rate will plants to compete for nitrogen. decrease (Ericsson, 1981; Ingestad and Improved growth of mycorrhizal plants Lund, 1986; Ingestad and Agren, 1988). probably results from a greater ion absorb- ing surface that increases nitrogen flux from a limited supply to the plant. In addi- Inorganic nitrogen uptake and utilization tion, the direct mineralization and cycling of nitrogen by the fungus are important Forest ecosystems contain large amounts (Vogt et al., 1982). However, in controlled of nitrogen, of which more than 90% is experimental systems when nitrogen addi- organically bound in plant and animal bio- tion rates were held constant, mycorrhizae mass, forest floor litter and soil. In did not increase nitrogen uptake even at contrast, plant growth depends upon the low levels of addition and decreased rela- uptake of inorganic nitrogen, usually less tive growth rate of pine seedlings, indicat- than 1 % of the total nitrogen present on ing a carbon drain (Ingestad et al., 1986). site (Carlyle, 1986). Competition for this The ammonium ion (NH+) is the first ion available nitrogen is intense, and higher released in mineralization, while nitrate plants have developed many strategies for (NOg) production (nitrification) is inhibited the acquisition and internal maintenance in many forest ecosystems (Keeney, 1980; of adequate levels. Vitousek and Matson, 1985). Although, Ammonium (NH+) and nitrate (N0 are under certain conditions, considerable ni- ) 3 trification can take place (Vitousek et aG, the major inorganic nitrogen ions in the soil and litter. The concentration of these 1982; Nadelhoffer et al., 1983; Smirnoff and Stewart, 1985). Because of the limited ions in the root zone is controlled by the production of NOand the intense compe- rate of mineralization and nitrification. tition for inorganic nitrogen, NH is the Roots of higher plants are usually concen- 4 trated in that portion of the soil profile in most common nitrogen form available to higher plants in some forest ecosystems. which maximum net mineralization is In undisturbed forests, the NH ratio 3 /NO 4 occurring (Eissenstat and Caldwell, 1988). is approximately 10:1 (Carlyle, 1986). Nitrogen mineralization is the biologically
However, tree species in other forest eco- important ecological and energetic impli- cations. Basic information in these systems and on different sites may be areas exposed to wide variations in the NH is severely lacking for forest trees. 3 /N0 4 ratio (Nadelhoffer et aL, 1985). wide range of Plants have evolved a contrasting life-forms and nutritional strat- Ammonium and nitrate ions differ great- because of the extreme environ- egies ly. Ammonium is the most reduced form of mental variability in NH and N0 availa- 4 3 nitrogen, while nitrate is the most oxidized; bility, the importance of maintaining an therefore, absorption of these ions is internal supply of N for growth and the affected differently by pH, temperature, ion importance of minimizing carbon costs of composition of the soil solution, carbohy- assimilation (Schulze, 1982; Chapin, drate supply in the roots and many other 1983; Chapin and Tryon, 1983). Little is factors (Bernardo et aL, 1984). Specific, known about differences in nutritional stra- active uptake systems are present in roots tegies among forest species on a particu- for both ions (Runge, 1983). However, lar site or within genera on different sites. passive diffusional uptake may also occur For example, different oak species are (Lee and Stewart, 1978). Once absorbed found on sites that differ widely in nitrogen by the root, NH is rapidly combined with 4 economies (relative NH availability). 3 :NO 4 glutamate to form glutamine, a major How do different species, such as north- transport and metabolically active amide ern red oak (Quercus rubra L.) or pin oak (Lee and Stewart, 1978; Pate, 1983; (Q. palustris Muenchh.), assimilate am- Runge, 1983; Kato, 1986). Little NH is4 monium or nitrate in response to differing translocated to shoots in the xylem. In environmental variables to maximize contrast, N0 may be translocated in 3 growth or competitive ability? xylem to stem or leaves before metabo- The ability to utilize both NH and N0 3 4 lism, stored within cells or reduced imme- differs widely among species. When sup- diately in the root by nitrate reductase. plied with NH NH or N0 species , :NO , 44 3 3 With nitrate reductase, N0 is reduced 3 of Alnus, Pinus, Picea and Pseudotsuga through a series of steps to NH then to , 4 grow best in the order NH > NH > 44 3 :NO some transport or storage organic nitrogen N0 Many plants (including tomato and - 3 compound (usually glutamine or aspara- certain weeds, like Chenopodium) grow gine). The functioning, location, carbon best with N0 > NH > NH (Runge, 344 3 :N0 costs and energetics of the nitrate reduc- 1983; Kato, 1986; Salsac et al., 1987). tase system have been the focus of many However, there is much contradictory lit- studies in crop plants and weeds (Smirnoff erature concerning growth and nitrogen and Stewart, 1985; Andrews, 1986; Kelt- source, even on the same species (Titus jens et al., 1986; Rufty and Volk, 1986; and Kang, 1982; Kato, 1986). Much of this MacKown, 1987), in fruit trees (Titus and controversy is related to uncontrolled Kang, 1982; Kato, 1986), and in forest experimental variables. For example, trees (Blacquiere and Troelstra, 1986; results of fertilizer experiments with NH 4 Wingsle al., 1987; Margolis et al., et or N0 in soils must be viewed with cau- 3 1988). The absorption and utilization of tion because nitrification rates are usually ammonium vs nitrate, the extent to which not controlled or measured. In addition, nitrate is reduced or stored in the root or large pH changes in solution culture or transported to leaves, the extent to which soils can result from differential uptake of it is reduced or stored in leaves, and the NH or N0 Even in buffered soils or . 3 kinds of transport and storage compounds 4 solution culture, steep pH gradients can involved for a particular species have
build up within and near roots. In unbuf- acids translocated from shoots to roots are fered NH solution culture, pH can de- phloem, converted into organic in the 4 crease from 7 to 3 within 48 h (Runge, nitrogen compounds and retranslocated back to shoots in the xylem (Dickson, 1983). Thus, without careful experimental 1979; Pate, 19130; 1983). The amount and control, growth differences attributed to kind of organic nitrogen compounds trans- different nitrogen sources may instead reflect the species response to extreme located in xylem differ with plant species pH and the associated changes in cation (Barnes, 1963; Pate, 1980), plant develop- and anion availability, rather than the mental stage, season of the year (Sauter, plant’s ability to assimilate different nitro- 1981; Tromp and Ovaa, 1985; Kato, gen sources. For example, metabolic iron 1986), the amount or kind of inorganic deficiency is common in some plants utiliz- nitrogen available to roots (Weissman, ing N0 High pH (above 6.5) in the root 1964; Peoples et al., 1986) and perhaps . 3 environment can inhibit iron uptake, while other environmental The factors. two high internal levels of organic acids may amides, asparagine and glutamine, are major transport compounds in trees and chelate and inactivate absorbed iron many other plants and move readily in (Runge, 1983). In contrast, high levels of NH can decrease soil pH and cation both xylem and phloem (Bollard, 1958; 4 uptake, increase loss of cations from root Pate, 1980; Dickson et al., 1985; Schubert tissue and lead to cation (e.g., K, Mg, Ca) 1986). In addition to glutamine and aspar- deficiencies (Boxman and Roelofs, 1988). agine, many other amino acids and ureides are transported in xylem (Barnes, Plants have many strategies for balanc- 1963; Titus and Kang, 1982; Kato, 1986). internal pH (Raven, 1985). The most ing Although 5-15 amino acids are commonly common is the production of organic found in xylem sap (Dickson, 1979), as acids. In this reaction, dark-fixation of C0 2 many as 25 amino acids and ninhydrin- generates H consumes OH- and pro- , + positive compounds have been found duces organic acids. These acids can be (Sauter, 1981; Kato, 1986). In spite of the precipitated (oxalic), stored in vacuoles or large number of amino compounds found transported back to the root along with K+ in xylem, only the amides, asparagine and in the phloem (Bown, 1985; Raven, 1985; glutamine; the amino acids, glutamate, Allen and Raven, 1987). The ability of a aspartate, arginine and proline; and the particular plant species to reduce nitrate in ureides, allantoin, allantoic acid and citrul- either roots or shoots, to produce organic line, are common and major transport transport cations to balance inter- acids, to compounds (Barnes, 1963; Pate, 1980; nal pH and adjust osmotically to to water Kato, 1986; Schubert, 1986). determines the ability to largely stress assimilate different nitrogen sources (Ar- The presence of a relatively large num- nozis and Findenegg, 1986; Salsac et al., ber of different amino compounds in xylem 1987). and phloem raises a number of important functional quesi:ions. The ureides and amides have low carbon/nitrogen ratios Organic nitrogen transport (e.g., allantoin, 1:1; citrulline, 2:1, aspara- gine, 2:1; giutamine, 2.5:1) and are effi- cient forms for storing and transporting Inorganic nitrogen taken up by roots is rapidly converted into organic nitrogen nitrogen in respect to carbon required. Asparagine also has the characteristics compounds for translocation within the (i.e., high solubilily, stability and mobility in plant. Sugars, organic acids and amino
xylem and phloem) required for efficient nitrogen compounds provide metabolic nitrogen transport. In contrast, arginine, an mechanisms for regulation of the nitrogen important nitrogen storage compound fre- composition of both xylem and phloem; for quently found in xylem sap, does not have uptake, distribution and recycling of nitro- the mobility of asparagine or glutamine. At gen within the plant; and for selective allo- xylem sap pH, arginine is absorbed onto cation of nitrogen to various sinks in the the cell walls and seems to move by plant. In forestry research, there is a criti- sequential cation exchange like calcium cal need for information about nitrogen transport in trees. Little is known about the (Pate, 1980). mechanism of uptake, metabolism and The transport of different amino acids in allocation of these compounds; the carbon is influenced by xylem sap pH (van xylem costs of uptake, metabolism and transport; Bel et al., 1981At xylem sap pH (usually and how these factors change with plant 5.5-6.0) the general uptake pattern is ontogeny and environmental stress. basic > neutral > acidic amino acids. Therefore, alanine and arginine are rapidly absorbed from the xylem free-space, while Organic nitrogen storage glutamic and aspartic acids move with the xylem sap into transpiring mature leaves. Because of this pH-regulated differential The temporary storage of carbon and uptake in xylem, three distributional pat- nitrogen is necessary for normal plant terns were found in cottonwood (Vogel- growth. The major cycles of nitrogen stor- mann et aL, 1985). 1) Alanine was taken age and utilization are seasonal and up and retained in the stem with little associated with changes in tree growth, transport to either phloem or developing although some diurnal cycling is found leaves. 2) Threonine and glutamine were (Dickson, 1987). These cycles have been removed from the xylem free-space in the studied mainly in fruit trees and have been stem and were transferred from primary recently reviewed (Glerum, 1980; Stassen xylem to secondary xylem, from xylem to et al., 1981; Titus and Kang, 1982; Tromp, phloem, and were then translocated to 1983; Kato, 1986). developing leaves in both xylem and In annual plants, considerable nitrate phloem. 3) Aspartic and glutamic acids and amino acids may accumulate in were not strongly absorbed by stem tissue leaves if nitrogen uptake exceeds growth but moved with the xylem sap into mature demands of the plant (Pate, 1983). In leaves. These amino acids were then addition, nitrogen can accumulate in vege- either metabolized in mature leaf tissue or tative tissue as proteins. Ribulose 1,5-bis- loaded into the phloem for retransport to phosphate carboxylase, the major func- developing leaf or stem and root sinks. tional protein in leaves, may be defined as Carbohydrate transport to roots, nitro- a storage protein in that it is accumulated gen uptake, production of amino acids, during vegetative growth and then hydroly- and transport back to shoots are closely zed and used in reproduction (Millard, controlled feedback cycles regulated by 1988). Specific storage proteins may also demand of both shoots and roots for car- accumulate in specialized mesophyll cells bohydrate and nitrogen necessary for of certain legumes (Franceschi et al.. growth. The differential production of 1983) These storage proteins are hydro- amino acids and other transport nitrogen lyzed during leaf senescence and the car- compounds in roots and the different dis- bon-nitrogen compounds released are tributional patterns in shoots of these used for seed production.
In perennial plants, nitrogen is stored ment of better extraction techniques, few both in soluble amino compounds and in detailed studies were conducted. Studies protein. There is controversy over whether on Salix (Sauter and Wellenkamp, 1988) soluble nitrogen compounds or proteins have shown that storage proteins are lo- important (Tromp, 1983). In cated in vacuoles of ray cells, and gel are more trees, in late November when pro- electrophoretic studies of these Salix pro- apple tein accumulation in bark peaked, Kang teins and others from ginkgo bark (Shim and Titus (1980) found about 90% of the and Titus, 1985) have begun to charac- nitrogen in protein and about 10% in terize these storage proteins. These pro- soluble amino compounds. The relative teins are rich in arginine and other basic proportions of soluble versus insoluble amino acids (Kang and Titus, 1980), accu- nitrogen compounds vary with the season, mulate in the fall, disappear in the spring within different parts of the tree, with fertili- and are glycoproteins similar to those zation, with different extraction methods found in soybean (Franceschi et al., and with changing environmental condi- 1983). However, little is known about tions (Kato, 1986). these storage proteins in trees. In-depth studies are clearly needed of their deposi- The major soluble nitrogen storage com- tion, hydrolysis, chemical composition and pounds are arginine, proline, asparagine response to fertilization and environmental and glutamine. The particular nitrogen stress. compounds accumulated are quite spe- cies specific, and different species may be Nitrogen storage usually begins as soon grouped according to the major free amino leaf and shoot growth slows in as new acid present during storage (Sagisaka and early summer. The initiation of storage is Araki, 1983). Arginine, proline or a combi- often indicated by an increase in arginine nation of these two amino acids are the concentration in small branches and bark major soluble nitrogen storage compounds tissue. Both soluble and protein nitrogen in most trees (Titus and Kang, 1982; Kato gradually increase during the summer as 1986). Although arginine is a major stor- growth slows, then rapidly increase as age amino acid, it is usually converted into leaves begin to senesce. Leaves on small asparagine or glutamine for transport from trees may contain up to 50% of the total storage tissue to new developing tissue nitrogen in the plant, and 75-80% of that (Tromp and Ovaa, 1979). These transfor- nitrogen may be retranslocated back into mations from storage to transport com- stems before leaf abscission (Chapin and pounds were inferred from changes in the Kedrowski, 1983; Cote and Dawson, concentrations of the individual amino 1986; Tyrrell and Boerner, 1987). Nitrogen acids. However, little is known about the accumulation continues late into the fall in specific metabolic reactions involved (Sie- the main stem and roots as soluble nitro- ciechowicz et al., 1988). Proline is the gen moves from twigs to main stem, and major soluble amino acid in dormant citrus newly absorbed inorganic nitrogen is (Kato, 1986). However, because proline is converted into organic nitrogen and stored not a carbon efficient storage compound in roots (Tromp, 1983; Kato, 1986). (C:N, 5:1), it must have some important In evergreen trees, leaves and needles metabolic function in dormant and well as steim and roots are important as stressed plants (Hanson and Hitz, 1982). sites for nitrogen storage. Nitrogen is The presence of storage proteins in tree stored during periods of inactive growth tissue has been recognized for a long and then retranslocated to new developing time. However, until the recent develop- leaves and shoots during flushing. In
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