These authors contributed equally to the present study.
Response pattern of amino compounds in phloem and xylem of trees to soil drought depends on drought intensity and root symbiosis
Article first published online: 30 JUL 2012
© 2012 German Botanical Society and The Royal Botanical Society of the Netherlands
Special Issue: Woody Plant Performance in a Changing Climate. Guest Editor: M.S. Günthardt-Goerg. The German Botanical Society, the Royal Botanical Society of the Netherlands and Wiley have published this supplement without financial support.
Volume 15, Issue Supplement s1, pages 101–108, January 2013
How to Cite
Liu, X.-P., Gong, C.-M., Fan, Y.-Y., Eiblmeier, M., Zhao, Z., Han, G. and Rennenberg, H. (2013), Response pattern of amino compounds in phloem and xylem of trees to soil drought depends on drought intensity and root symbiosis. Plant Biology, 15: 101–108. doi: 10.1111/j.1438-8677.2012.00647.x
Editor M. Günthardt-Goerg
- Issue published online: 21 DEC 2012
- Article first published online: 30 JUL 2012
- Received: 31 January 2012; Accepted: 1 June 2012
- Amino compounds;
- drought stress;
- long-distance transport;
- nitrogen nutrition;
- symbiotic N fixation
This study aimed to identify drought-mediated differences in amino nitrogen (N) composition and content of xylem and phloem in trees having different symbiotic N2-fixing bacteria. Under controlled water availability, 1-year-old seedlings of Robinia pseudoacacia (nodules with Rhizobium), Hippophae rhamnoides (symbiosis with Frankia) and Buddleja alternifolia (no such root symbiosis) were exposed to control, medium drought and severe drought, corresponding soil water content of 70–75%, 45–50% and 30–35% of field capacity, respectively. Composition and content of amino compounds in xylem sap and phloem exudates were analysed as a measure of N nutrition. Drought strongly reduced biomass accumulation in all species, but amino N content in xylem and phloem remained unaffected only in R. pseudoacacia. In H. rhamnoides and B. alternifolia, amino N in phloem remained constant, but increased in xylem of both species in response to drought. There were differences in composition of amino compounds in xylem and phloem of the three species in response to drought. Proline concentrations in long-distance transport pathways of all three species were very low, below the limit of detection in phloem of H. rhamnoides and in phloem and xylem of B. alternifolia. Apparently, drought-mediated changes in N composition were much more connected with species-specific changes in C:N ratios. Irrespective of soil water content, the two species with root symbioses did not show similar features for the different types of symbiosis, neither in N composition nor in N content. There was no immediate correlation between symbiotic N fixation and drought-mediated changes in amino N in the transport pathways.
Many forest ecosystems have developed and evolved on marginal soils, characterised by low availability of essential nutrients such as phosphorus and nitrogen (N) (Raven & Andrews 2010). This is not only true for forests in the tropics, but also for forests in the temperate zone; in particular on limestone-derived soils that are often nutrient-poor and have low water-holding capacity (Geßler et al. 2007; Kreuzwieser & Geßler 2010). Since these forests can have high productivity on marginal soils, it has been speculated that the perennial lifestyle is an adaptation to low-nutrient availability (Rennenberg & Schmidt 2010).
Nevertheless, N availability in soil is a main nutritional factor that restricts tree growth and development in forests of the temperate zone (Tamm 1991). Mostly from studies on agricultural plants, it has long been assumed that nitrate is the dominant source of soil-derived N in plants (Andrews 1986; Gebauer & Stadler 1990; Gojon et al. 1994; Truax et al. 1994). However, recent studies show that: (i) this neither holds for many temperate forest tree species (Rennenberg et al. 2009) nor all agricultural plants (e.g. Robinson et al. 2011); and (ii) in addition to ammonium (NH4), amino compounds constitute an important soil-derived N source in plants (Näsholm et al. 2009). Plant exploitation of the soil and use of a variety of soil N sources strongly increase under N limitation through root symbiosis with mycorrhizal fungi and bacteria (Miransari 2011; Wu 2011). In addition, symbiotic fixation of atmospheric N2 in the roots using rhizobial or actinorhizal symbioses can improve plant N uptake on marginal soils (Hedin et al. 2009).
Within a plant, the diversity of soil-derived N sources and their assimilation affect N composition of the transport pathways between the root and shoot, i.e. the xylem and phloem (Herschbach et al. 2012). For example, trees such as Norway spruce (Picea abies L.) and European beech (Fagus sylvatica L.) that preferentially take up reduced N sources, rather than nitrate, and assimilate N preferentially through the roots have low nitrate and NH4 but high amino N content in both xylem and phloem (Schneider et al. 1996; Geßler et al. 1998). The amino N pools in xylem and phloem can be expanded or depleted, depending on N availability in the soil, environmental factors that affect soil N acquisition and developmental processes that consume N (Rennenberg et al. 1998; Rennenberg & Geßler 1999; Herschbach et al. 2012). Therefore, these N pools may indicate the state of N nutrition in trees. In this context, amino N in the xylem can be taken as a measure of N supply to the shoot, amino N in the phloem as a measure of reallocation of excess N to roots (Herschbach et al. 2012), which can also regulate N uptake processes in roots (Geßler et al. 2004a).
Trees exposed to intense drying–wetting cycles, e.g. as a consequence of global climate change (Kreuzwieser & Geßler 2010), or when growing in dry environments, are particularly prone to serious N deficiency because of (i) low soil organic matter, (ii) wind and water erosion, (iii) decreased movement of soil N sources to the root surface (Cairns et al. 2011) and (iv) decreased N turnover in leaf and root litter (Berg & Laskowski 2006). At the whole plant level, soil water deficiency leads to a decrease in plant water content, transpirative sap flow and, hence, nutrient allocation from root to shoot (Fig. 1). In addition to N uptake, xylem loading and plant internal cycling of amino N between roots and shoots can be inhibited (Fig. 1), resulting in decreased N availability for growth and development (Fotelli et al. 2002; Herschbach et al. 2012). The content of soluble N compounds transported in the phloem and xylem of trees can be reduced and its composition changed under these conditions in favour of compatible solutes such as proline (Pro) (Geßler et al. 2004b; Nahm et al. 2007; Herschbach et al. 2012). However, whether such changes depend on drought intensity and/or growth reduction caused by drought has not been elucidated. Moreover, drought may transiently improve N nutrition of trees due to enhanced liberation of N from decaying microbial biomass (Dannenmann et al. 2009).
It has frequently been assumed that the negative effects of drought on N nutrition can be reduced by root symbiotic relationships; however, experimental evidence is scarce. This may be because mycorrhizal fungi and rhizobial or actinorhizal bacteria are themselves drought sensitive (Lehto & Zwiazek 2011; Miransari 2011; Sadok & Sinclair 2011) and this sensitivity may affect symbiotic N nutrition. The aim of the present study was to identify drought-mediated differences in amino N composition and content of xylem and phloem in species with different types of symbioses with N2-fixing bacteria. Robinia pseudoacacia, Hippophae rhamnoides and Buddleja alternifolia were chosen for this study because they are important tree species for reforestation in arid and semiarid areas of northwest China. R. pseudoacacia can build nodules with Rhizobium spp.; H. rhamnoides, an important economic shrub, can fix atmospheric N2 by building actinorhizal symbiosis with Frankia spp.; and B. alternifolia does not have symbiotic relationships with atmospheric N2-fixing bacteria. In an experiment under controlled conditions, the following research questions were addressed: (i) is N nutrition balanced with drought-mediated changes in growth and, hence, is amino N content in xylem and phloem affected by drought; (ii) does drought alter the composition of amino N in the xylem and phloem in favour of compatible solutes such as Pro; and (iii) do root symbioses with atmospheric N2-fixing bacteria prevent drought-mediated changes in amino N allocation to the xylem?
Material and methods
Plant material and treatments
At the end of March 2008, 1-year-old seedlings of R. pseudoacacia, H. rhamnoides and B. alternifolia were transferred individually to pots (50-cm high, diameter 35 cm, volume = 48 l) filled with mineral field soil, with 0.039% total N, 11.18 mg·kg−1 NH4+-N and 13.55 mg·kg−1 NO3−-N, on a dry weight basis. A water-permeable tube of 10 mm in diameter, reaching from the substrate surface to the pot base, was buried in the substrate and used for watering to ensure equal distribution of water inside the pot. After planting, shoots of the seedlings were cut 3–5 cm above the soil surface, a technique often used in afforestation of dry areas, to promote seedling survival and growth in the early phases of development.
The plants were grown outside under a rain shelter to avoid rainfall impact on soil water content. Meteorological conditions during the experiment are shown in Table 1. From the end of May, seedlings of each species were exposed to one of three soil water conditions: suitable soil water content (70–75% of field capacity), medium drought (45–50%) and severe drought (30–35%) (n = 6–8 for each treatment). Based on the weight of the pot, the substrate, seedling and defined soil water content, the weight of a pot for a given soil water treatment was determined. Soil water content in a pot was maintained by weighing the pot and compensating for water lost through transpiration up to a fixed weight at dusk through addition of tap water. In mid-August, plants were harvested from 09:00 to 17:00 h over two consecutive days with similar weather conditions. To avoid the impact of diurnal fluctuations in environmental conditions on sampling, one plant from each treatment was harvested followed by the next plant from each treatment in the same order. Whole plant biomass was determined by weighing. Roots inspected at harvest, indicated a high abundance of nodules on R. pseudoacacia and full symbiosis with Frankia on H. rhamnoides, but no indication of symbiosis on roots of B. alternifolia.
|highest day temperature (ºC)||lowest night temperature (ºC)||average daily sunshine (h)||maximum daily PAR (μmol photons m−2 s−1)|
Collection of xylem sap and phloem exudate
Xylem sap of seedlings was collected using a modification of the procedure of Scholander et al. (1965) described in Rennenberg et al. (1996). It mid-August, shoots of six individuals of each tree species from each treatment were cut 6–8 cm above the soil surface. Small pieces of bark and cambium (20–25 mm) were removed from the cut end and the stripped end rinsed thoroughly with double-distilled water to reduce contamination with cellular constituents. Xylem sap of shoots was collected using a pressure chamber (Soil Moisture Inc., Santa Barbara, CA, USA) by raising the pressure to 0.5 MPa above shoot water potential for 2 min. The first droplets were discarded to avoid contamination; the collected xylem sap was immediately frozen in liquid N2 and stored at −80 °C until analysis.
Phloem exudates were collected by a modification of the bark exudation/EDTA technique (King & Zeevart 1974) described in Rennenberg et al. (1996). During collection of xylem sap, small pieces of bark (ca. 30–50 mg fresh weight) were removed from the cut end of the shoot of each harvested tree (n = 6–8) and, after weighing, placed in an exudation solution containing 10 mm EDTA and 0.015 mm chloramphenicol (pH 7.0). Bark pieces were incubated in this solution at room temperature for 5 h. Subsequently, pieces were removed, phloem exudate frozen in liquid N2 and stored at −80 °C until analysis.
Analysis of amino compound composition and content in phloem and xylem
In order to analyse the composition and content of amino compounds, xylem sap and phloem exudate were centrifuged at 14,000 g and 4 °C for 5 min. After adjustment with HCl to pH 2.2–2.5, aliquots of 50 μl of clear supernatant were injected into a Waters Acquity UPLC system (Waters Corp., Milford, MA, USA) and separated and quantified with a standard protocol at a column temperature of 61 °C (Luo et al. 2009). Amino acid standards H (NCI0180; Pierce Biotechnology, Inc., Rockford, IL, USA) were used as standard. According to composition of the samples, additional amino compounds were added to this standard as required at 2.5 mmol in 0.1 N HCl each. Total content of amino N in phloem and xylem was summed based on the concentration and molar N content of the individual amino compounds.
Significant differences in individual amino compounds between treatments (n = 5–6) were analysed with the program SPSS 16.0 for Windows (SPSS Inc., Chicago, IL, USA). Prior to testing significance with the Turkey test, normality and homogeneity of data were tested with the Kolmogorov–Smirnov and Levene test, respectively; differences were considered significant at P < 0.05.
Total plant biomass of R. pseudoacacia was significant higher than that of H. rhamnoides and B. alternifolia under all soil water treatments (Table 2). There was no distinct difference in biomass between H. rhamnoides and B. alternifolia irrespective of water supply. Increasing drought led to a gradual decrease in total plant biomass of all three tree species. The relative decline mediated by medium drought was more pronounced for R. pseudoacacia compared to the other two species, but was similar for all three species under severe drought.
|soil water content||R. pseudoacacia||H. rhamnoides||B. alternifolia|
|g plant−1/%||shoot/root||g plant−1/%||shoot/root||g plant−1/%||shoot/root|
|70%||162 ± 31Bb 100 ± 19Ab||2.4 ± 0.5Ab||74 ± 18Ab 100 ± 24Ab||3.1 ± 0.3Aa||76 ± 27Ab 100 ± 36Aa||3.1 ± 0.4Ab|
|50%||94 ± 13Ba 58 ± 14Aa||2.3 ± 0.6Aa||55 ± 15Aab 75 ± 27Aab||4.0 ± 0.8Bab||60 ± 18Aab 78 ± 29Aa||2.8 ± 0.5Aa|
|35%||72 ± 20Ba 44 ± 28Aa||1.5 ± 0.5Aa||32 ± 12Aa 44 ± 34Aa||6.0 ± 2.0Cb||46 ± 16Aa 60 ± 35Aa||2.3 ± 0.3Ba|
Under suitable soil water condition, the shoot/root ratio of R. pseudoacacia was slightly lower than that of H. rhamnoides and B. alternifolia, but the difference was not statistically significant (Table 2). Under drought, the shoot/root ratio of H. rhamnoides increased, while that of R. pseudoacacia and B. alternifolia declined. Consequently, the shoot/root ratio of R. pseudoacacia and B. alternifolia was significantly lower than that of H. rhamnoides under drought conditions. These results indicate a significant difference between the three tree species in the shoot/root ratio in response to soil water deprivation.
Effect of soil water content on composition and content of amino compounds in phloem and xylem
Under suitable soil water conditions, the dominant amino compounds in phloem and xylem of R. pseudoacacia seedlings were asparagine (Asn) and γ-amino-n-butyric acid (GABA) (Figs 2 and 3A,B); with high levels of alanine (Ala) and NH4+ in the phloem (Figs 2 and 3A) and sarcosine (Sarc) in the xylem (Figs 2 and 3B), but the Ala level in the xylem was very low. β-Ala and ethylamine were not found in phloem exudates, but were present in the xylem sap. When seedlings were grown under medium drought, Asn and GABA were still the dominant amino compounds in phloem and xylem; the Asn concentration in phloem (Fig. 3C) and GABA concentration in xylem (Fig. 3D) increased significantly in response to medium drought. The phloem also contained enhanced concentrations of proline (Pro), arginine (Arg) and 3-methyl histidine (3-M-his) in response to medium drought, whereas the Ala concentration decreased significantly (Fig. 3C). In xylem, levels of glutamine (Gln) and Sarc decreased and Pro increased significantly in response to medium drought (Fig. 3D). When seedlings were exposed to severe soil drought, Asn was still the dominant amino acid in phloem, while Arg was dominant in phloem due to a strong increase in concentration (Fig. 3E). Levels of Ala and GABA in phloem were significantly lower compared to the well-watered control, and Pro concentration dropped below the limit of detection under severe drought. In xylem, concentrations of Asp, threonine (Thr), Asn, Gln, Sarc and histidine (His) decreased, whereas Pro increased significantly (Fig. 3F).
Under all soil water contents, NH4+ concentration was relatively high in phloem and xylem. The concentration in phloem tended to decrease with increasing soil drought, while in xylem, NH4+ levels increased significantly under medium drought, but remained at control levels under severe drought. Drought did not have significant effects on the total amino N in the long-distance transport pathways of R. pseudoacacia (Fig. 4A).
Under all soil water treatments, Asn was the only dominant amino compound in the phloem and xylem of H. rhamnoides seedlings (Fig. 5). In addition, α-aminodiphenylamine (α-aminodip), which was not found in R. pseudoacacia, had a relatively high concentration in the phloem and xylem of H. rhamnoides, irrespective of the soil water treatment. Sarc, which was one of main amino compounds in the xylem of R. pseudoacacia, was not found in the xylem of H. rhamnoides. The Pro level was below the limit of detection in the phloem of H. rhamnoides and was also very low in the xylem. Differences of soil water content did not have a significant effect on NH4+ level in phloem and xylem.
Under medium drought, the levels of serine (Ser), Asn, Gln, methionine (Met), ethylamine and His in the phloem dropped significantly, and no positive effects were observed (Fig. 5C). In xylem, the concentrations of Asp and Asn increased significantly, and no negative effects were observed (Fig. 5D). Severe drought significantly reduced the concentrations of Asn, GABA, Met and ethylamine in the phloem, but increased the levels of Thr, Ser, Asn, α-aminodip and α-aminobenzene sulphonamide (α-aminobs) in the xylem (Fig. 5E,F).
Compared to the well-watered control, H. rhamnoides seedlings grown under medium and severe droughts showed a slight, but not significant, decrease in total content of amino N in the phloem (Fig. 4B). In xylem, the total content of amino N increased with increasing drought stress; this increase was statistically significant under the severe drought.
Unlike the other two species studied, the dominant amino compounds under suitable water supply in B. alternifolia were GABA and Arg in the phloem and Arg in the xylem (Figs 2 and 6A,B). The level of Arg in both transport fluids was significantly higher than in R. pseudoacacia and H. rhamnoides. Asn was not a dominant amino compound in the phloem and xylem of B. alternifolia, in contrast to R. pseudoacacia and H. rhamnoides. Sarc or α-aminodip, which were main amino compounds in the phloem of R. pseudoacacia or H. rhamnoides, respectively, were below the limit of detection in the phloem of B. alternifolia. Leucine (Leu) and phenylalanine (Phe) were found in the phloem of B. alternifolia, but not in R. pseudoacacia and H. rhamnoides. Under all soil water treatments, Pro levels in the phloem and xylem of B. alternifolia were very low (Fig. 6). In response to medium and severe drought, the only dominant amino compounds were GABA in the phloem and Gln in the xylem of B. alternifolia seedlings. Under medium drought, the Arg level in the phloem of B. alternifolia dropped significantly, but the concentrations of Asp, glutamic acid (Glu) and ethylamine increased significantly (Fig. 6C). In xylem, the Gln level increased, while the Arg level decreased significantly in response to medium drought (Fig. 6D); in addition, the levels of Ser and Glu in the xylem declined significantly. Under severe drought, the levels of Asn, Glu, Arg and NH4 decreased significantly in the phloem (Fig. 6E). In the xylem, responses of amino compounds to severe drought (Fig. 6F) were similar to those for the medium drought treatment (Fig. 6D). Ethylamine, which was not found in the xylem of well-watered controls, was present in the xylem of B. alternifolia seedlings grown under medium and severe drought stress, and showed a relatively high level under severe drought. Also, a significant increase in the NH4 level was observed in response to severe drought.
Total content of amino N in the phloem and xylem of B. alternifolia tended to a decrease under medium drought, but increased under severe drought (Fig. 4C). However, these effects were statistically significant only for xylem in the severe drought treatment. In the phloem, total amino N was similar to observed for H. rhamnoides, but much lower than in R. pseudoacacia. Total amino N in the xylem of B. alternifolia was similar to that found in H. rhamnoides and R. pseudoacacia.
In previous studies, variations in N metabolism in response to drought stress were reflected in the composition and concentration of individual amino compounds in the phloem and xylem, indicating a drought-induced unbalance between N metabolism and growth. Responses differed at different intensities of drought stress and between tree species (Fotelli et al. 2002; Geßler et al. 2004b). The present experiments indicate that in seedlings of R. pseudoacacia N nutrition is very well adapted to drought-mediated changes in growth. Drought strongly reduced biomass accumulation of the seedlings, largely at the expense of shoot growth, but amino N content of the xylem – a measure of N supply to leaves and, hence, N nutrition – and the phloem – a measure of reallocation of amino N not used by the leaves – remained unaffected by the drought treatments. However, the composition of amino compounds in the xylem and phloem changed in response to drought in different ways. In the phloem of R. pseudoacacia, drought favoured amino compounds with a low C/N ratio, in particular Arg containing 4 Mol·N·Mol−1, indicating a reduced investment of C in N reallocation. A similar effect of drought was not observed in composition of the xylem. Arg accumulation was also observed in leaves of mistletoes, which are C-limited due to limited photosynthetic carbon assimilation capacity (Escher et al. 2004). Apparently, the incorporation of excess N into Arg during C limitation is a more general strategy.
Unlike results with R. pseudoacacia, in H. rhamnoides and B. alternifolia only the content of amino N in the phloem remained constant in response to drought, whereas amino N content in the xylem increased in both of these species. This surprising effect of drought was unexpected, since drought stress has previously been described to result in a reduction in N uptake and internal N availability (Imsande & Touraine 1994; Fotelli et al. 2002; Geßler et al. 2004b). The present observations seem to be independent of root symbiosis, since H. rhamnoides has symbiosis with actinomycetes, but B. alternifolia has no symbiosis; moreover, this effect was not observed in R. pseudoacacia, which develops symbiosis with Rhizobium spp. for N2 fixation. Furthermore, increased N content in the xylem in response to drought cannot be attributed to changes in the shoot/root ratio, since biomass accumulation declined in response to drought in H. rhamnoides (surprisingly) in favour of the shoot and in B. alternifolia (as expected) in favour of the root.
The increased amino N content in the xylem can be explained through different drought-mediated processes. (i) Drought may more strongly affect C assimilation, and hence biomass accumulation, than N uptake and N assimilation, resulting in an unbalanced C:N budget reflected by enhanced amino N content in the xylem. This imbalance may be caused by a stronger reduction in transpiration compared to xylem loading with amino compounds, or a stronger reduction in xylem unloading compared to transpiration. (ii) Drought may induce protein degradation in the roots and stem as a consequence of insufficient N uptake; part of the amino N generated from this degradation may be transported in xylem to the leaves, and this allocation is reflected in enhanced amino N content of the xylem (Herschbach et al. 2012). (iii) Alternatively, enhanced amino N content of the xylem could be a consequence of complex plant–microbial interactions in the rhizosphere. Drought will reduce C allocation to, and exudation from, roots resulting in a decline in microbial biomass. This decline may transiently liberate additional N into the soil, and roots may take advantage of this additional N source by enhanced uptake under drought conditions. This phenomenon has been observed in field experiments with European beech (Dannenmann et al. 2009) and may result in transiently improved N nutrition despite drought, as indicated by enhanced amino N content in the xylem.
As in R. pseudoacacia, the composition of amino compounds in the xylem and phloem of H. rhamnoides changed in response to drought in different ways. However, unlike R. pseudoacacia, drought favoured the amide Asn in the xylem and not in the phloem, indicating a reduced investment of C in N allocation from the roots to the shoot. Also, the changes in amino N composition in response to drought were more severe in the xylem compared to the phloem. In the xylem of B. alternifolia, an increase in Gln-N was almost compensated by a decrease in Arg-N, indicating a largely unchanged investment in C per N allocation from roots to the shoot. However, the switch from Arg to Gln can be ascribed to a metabolic change from N storage to N mobilisation; this has been observed during seasonal N cycling (Herschbach et al. 2012). Numerous studies have shown that Arg is dominant during winter dormancy (Sauter & van Cleve 1992; Schneider et al. 1994), whereas in spring Gln is the main amino compound in bark and xylem sap of poplar (Sauter & van Cleve 1992; Schneider et al. 1994) and other tree species (Adams et al. 1995; Schneider et al. 1996; Geßler et al. 1998; Plassard et al. 2000; Grassi et al. 2002).
Proline is considered to be an important compatible solute in plants, and fluctuations in its concentration are often closely related to drought resistance and to changes in N uptake and assimilation of newly absorbed N (Lee et al. 2009). In the present study, Pro concentrations in the long-distance transport pathways of all three species analysed were very low, and even below the limits of detection in phloem of H. rhamnoides and in phloem and xylem of B. alternifolia. Hence, the function of Pro as compatible solute in drought resistance seems to be limited in the studied tree species.
The tree species analysed mainly showed individual responses to drought in the composition of amino N in xylem sap and phloem exudate. In particular, the two species having symbiotic N2 fixation in the roots did not show similar features, neither in N composition nor in N content. However, R. pseudoacacia contained a significantly higher N content in xylem and phloem under well-watered conditions compared to the two other species studied. On exposure to drought, N content in the xylem of N2-fixing H. rhamnoides reached the level of well-watered R. pseudoacacia, whereas the non-N2-fixing B. alternifolia strongly exceeded this level. Apparently, there is no immediate correlation between symbiotic N2 fixation and drought-mediated changes in amino N composition and content in the phloem and xylem of the three tree species.
In conclusion, N nutrition was balanced to drought-mediated changes in growth; hence, amino N content in the xylem and phloem were not affected by drought in R. pseudoacacia, but were in the two other species investigated. Drought did not alter the composition of amino N in the xylem and phloem in favour of compatible solutes such as Pro. Root symbioses with atmospheric N2-fixing bacteria did not prevent drought-mediated changes in amino N allocation in the xylem.
This study was funded by the National Natural Science Foundation of China (30972335), the International Science & Technology Cooperation Program of China (2010DFA04410), an international project (TS2010XBNL063) and the ‘111’ Project of the Education Ministry of China (B12007), as well as a grant from the Deutsche Forschungsgemeinschaft to X.L.
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