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Sex-specific carbon and nitrogen partitioning under N deposition in Populus cathayana

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Abstract

Key message

Females of Populus cathayana allocated increased N to soluble proteins, while males keep N allocation pattern unchanged under N enrichment.

Abstract

In our study, Populus cathayana as a model species is employed to detect the sex-specific responses in growth, photosynthetic nitrogen (N) use efficiency (PNUE), carbon (C) and N partitioning when exposed to 0, 7.5 and 15 g N m−2 year−1 on the basis of local N deposition level. Our results showed that females had higher responses in photosynthesis and growth than males when exposed to N deposition, and also exhibited higher PNUE than males when exposed to high level of N deposition, suggesting that plasticity in the females may enhance the capacity of young seedlings to acquire resources. Moreover, we found that females mainly allocated increased N to soluble proteins and detergent-soluble proteins, but not to cell-wall proteins, while males maintained original partitioning pattern of N and also accumulated excessive N in the form of free amino acids. Females also allocated more fraction of leaf N to carboxylation (P C), bioenergetics (P B), and then more fraction of leaf N to all components of photosynthetic machinery (P T) than males under high level of N deposition. Such sex-specific N allocation strategy may correlate with sex-related PNUE. These results indicated that there is a higher critical N demand in females, and females could use N nutrient more efficiently than males under high N deposition. We also found that higher shift from starch to soluble sugars, such as sucrose, occurred in females than in males under N enrichment. By contrast, excessive accumulation of starch and non-structural carbohydrate in females relative to males was observed under control conditions, which might inhibit female photosynthesis rate. Accordingly, we suggested that the different leaf C and N partitioning patterns could explain the sex-specific responses in growth. Therefore, females may obtain advantageous position in the process of intraspecific competition when exposed to high level of N deposition because they have higher light capture (total leaf area) ability and utilization efficiency (PNUE) than the males that confer the ability for fast growth and thus are likely to be more responsive to N enrichment. Our results suggested that it could be important to look at the stronger growth response of the females over the males under N enrichment at both the leaf and the plant scale.

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Abbreviations

BD:

Basal diameter

C:

Carbon

Chl:

Chlorophyll content

DMA:

Dry matter accumulation

FAA:

Free amino acids

LA:

Leaf area

N:

Nitrogen

Na :

Leaf N concentration on area basis

Nm :

Leaf N concentration on mass basis

NSC:

Non-structural carbohydrate

P C :

The fraction of leaf N allocated to carboxylation

P B :

The fraction of leaf N allocated to bioenergetics

P C+B :

The fraction of leaf N allocated to both carboxylation and bioenergetics

P L :

The fraction of leaf N allocated to light-harvesting components

P n :

Net photosynthetic rate

PNUE:

Photosynthetic N use efficiency

PPFD:

Photosynthetic photon flux density

P T :

The fraction of leaf N allocated to all components of photosynthetic machinery

SDS:

Sodium dodecyl sulfate

SH:

Shoot height

References

  • Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37

    Article  CAS  Google Scholar 

  • Araya T, Noguchi K, Terashima I (2006) Effects of carbohydrate accumulation on photosynthesis differ between sink and source leaves of Phaseolus vulgaris L. Plant Cell Physiol 47:644–652

    Article  CAS  PubMed  Google Scholar 

  • Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67

    Article  Google Scholar 

  • Brown KR, Thompson WA, Camm EL, Hawkins BJ, Guy RD (1996) Effects of N addition rates on the productivity of Picea sitchensis, Thuja plicata, and Tsuga heterophylla seedlings. II: photosynthesis, 13C discrimination and N partitioning in foliage. Trees Struct Funct 10:198–205

    Article  Google Scholar 

  • Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Chen L, Zhang S, Zhao H, Korpelainen H, Li C (2010) Sex-related adaptive responses to interaction of drought and salinity in Populus yunnanensis. Plant Cell Environ 33:1767–1778

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Han Y, Jiang H, Korpelainen H, Li C (2011) Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot 62:5037–5050

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cipollini ML, Whigham DF (1994) Sexual dimorphism and cost of reproduction in the dioecious shrub Lindera benzoin (Lauraceae). Am J Bot 81:65–75

    Article  Google Scholar 

  • Cooke JEK, Martin TA, Davis JM (2005) Short-term physiological and developmental responses to nitrogen availability in hybrid poplar. New Phytol 167:41–52

    Article  CAS  PubMed  Google Scholar 

  • Correia I, Nunes A, Duarte IF, Barros A, Delgadillo I (2005) Sorghum fermentation followed by spectroscopic techniques. Food Chem 90:853–859

    Article  CAS  Google Scholar 

  • Dawson TE, Bliss LC (1989) Patterns of water use and the tissue water relations in the dioecious shrub, Salix arctica: the physiological basis for habitat partitioning between the sexes. Oecologia 79:332–343

    Article  CAS  PubMed  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer Negundo. Ecology 74:798–815

    Article  Google Scholar 

  • Delph LF, Gehring JL, Arntz AM, Levri M, Frey FM (2005) Genetic correlations with floral display lead to sexual dimorphism in the cost of reproduction. Am Nat 166:S31–S41

    Article  PubMed  Google Scholar 

  • Dietrich R, Ploß K, Heil M (2004) Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant Cell Environ 27:896–906

    Article  CAS  Google Scholar 

  • Duan B, Xuan Z, Zhang X, Korpelainen H, Li C (2008) Interactions between drought, ABA application and supplemental UV-B in Populus yunnanensis. Physiol Plant 134:257–269

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Dudley LS, Galen C (2007) Stage-dependent patterns of drought tolerance and gas exchange vary between sexes in the alpine willow, Salix glauca. Oecologia 153:1–9

    Article  PubMed  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345

    Article  CAS  Google Scholar 

  • Farrar J, Pollock C, Gallagher J (2000) Sucrose and the integration of metabolism in vascular plants. Plant Sci 154:1–11

    Article  CAS  PubMed  Google Scholar 

  • Feng YL (2008) Nitrogen allocation and partitioning in invasive and native Eupatorium species. Physiol Plant 132:350–358

    Article  CAS  PubMed  Google Scholar 

  • Feng YL, Lei YB, Wang RF, Callaway RM, Valiente-Banuet A, Inderjit, Li YP, Zheng YL (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci USA 106:1853–1856

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  • Gehring JL, Monson RK (1994) Sexual differences in gas exchange and response to environmental stress in dioecious Silene latifolia (Caryophyllaceae). Am J Bot 81:166–174

    Article  Google Scholar 

  • Glynn C, Herms DA, Egawa M, Hansen R, Mattson WJ (2003) Effects of nutrient availability on biomass allocation as well as constitutive and rapid induced herbivore resistance in poplar. Oikos 101:385–397

    Article  CAS  Google Scholar 

  • Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV, Poulton PR, Willison TW (1998) Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol 139:49–58

    Article  CAS  Google Scholar 

  • Grassi G, Meir P, Cromer R, Tompkins D, Jarvis PG (2002) Photosynthetic parameters in seedlings of Eucalyptus grandis as affected by rate of nitrogen supply. Plant Cell Environ 25:1677–1688

    Article  Google Scholar 

  • Green TH, Mitchell RJ, Gjerstad DH (1994) Effects of nitrogen on the response of loblolly pine to drought. New Phytol 128:145–152

    Article  CAS  Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296

    Article  CAS  PubMed  Google Scholar 

  • Hacke UG, Plavcová L, Almeida-Rodriguez A, King-Jones S, Zhou W, Cooke JEK (2010) Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiol 30:1016–1025

    Article  CAS  PubMed  Google Scholar 

  • Hesse E, Pannell JR (2011) Sexual dimorphism in a dioecious population of the wind-pollinated herb Mercurialis annua: the interactive effects of resource availability and competition. Ann Bot 107:1039–1045

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiang H, Peng S, Zhang S, Li X, Korpelainen H, Li C (2012) Transcriptional profiling analysis in Populus yunnanensis provides insights into molecular mechanisms of sexual differences in salinity tolerance. J Exp Bot 63:3709–3726

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leigh A, Cosgrove MJ, Nicotra AB (2006) Reproductive allocation in a gender dimorphic shrub: anomalous female investment in Gynatrix pulchella? J Ecol 94:1261–1271

    Article  Google Scholar 

  • Li CY, Xu G, Zang RG, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406

    Article  CAS  PubMed  Google Scholar 

  • Lorenc-Plucinska G, Stobrawa K (2005) Acclimation of poplar trees to heavy metals in polluted habitats: I. Carbohydrate metabolism in fine roots of Populus deltoides. Acta Soc Bot Pol 74:11–16

    Article  CAS  Google Scholar 

  • Magill AH, Aber JD, Hendricks JJ, Bowden RD, Melillo JM, Steudler PA (1997) Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol Appl 7:402–415

    Article  Google Scholar 

  • Markwell JP, Thornber JP, Boggs RT (1979) Higher plant chloroplasts: evidence that all the chlorophyll exists as chlorophyll-protein complexes. Proc Natl Acad Sci USA 76:1233–1235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McGrath R (1972) Protein measurement by ninhydrin determination of amino acids released by alkaline hydrolysis. Anal Biochem 49:95–102

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Way DA (2011) Tree competition and defense against herbivores: currency matters when counting the cost. Tree Physiol 31:579–581

    Article  PubMed  Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757

    Article  PubMed  Google Scholar 

  • Montesinos D, Villar-Salvador P, García-Fayos P, Verdú M (2012) Genders in Juniperus thurifera have different functional responses to variations in nutrient availability. New Phytol 193:705–712

    Article  CAS  PubMed  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Chemical and microbiological properties. American Society of Agronomy, Madison, pp 539–579

    Google Scholar 

  • Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866

    Article  Google Scholar 

  • Obeso JR, Alvarez-Santullano M, Retuerto R (1998) Sex ratios, size distributions, and sexual dimorphism in the dioecious tree Ilex aquifolium (Aquifoliaceae). Am J Bot 85:1602–1608

    Article  CAS  PubMed  Google Scholar 

  • Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425

    Article  Google Scholar 

  • Paul-Victor C, Züst T, Rees M, Kliebenstein DJ, Turnbull LA (2010) A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana. New Phytol 187:1102–1111

    Article  PubMed  Google Scholar 

  • Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MR, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Global Change Biol 12:470–476

    Article  Google Scholar 

  • Pugnaire FI, Chapin FS III (1993) Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74:124–129

    Article  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606

    Article  Google Scholar 

  • Retuerto R, Lema BF, Roiloa SR, Obeso JR (2000) Gender, light and water effects in carbon isotope discrimination, and growth rates in the dioecious tree Ilex aquifolium. Funct Ecol 14:529–537

    Article  Google Scholar 

  • Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiol 23:137–144

    Article  PubMed  Google Scholar 

  • Rogers SR, Eppley SM (2012) Testing the interaction between inter-sexual competition and phosphorus availability in a dioecious grass. Botany 90:1–7

    Article  Google Scholar 

  • Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91:679–684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simon J, Gleadow RM, Woodrow IE (2010) Allocation of nitrogen to chemical defence and plant functional traits is constrained by soil N. Tree Physiol 30:1111–1117

    Article  CAS  PubMed  Google Scholar 

  • Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–475

    Article  CAS  PubMed  Google Scholar 

  • Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879

    Article  CAS  PubMed  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • Vitousek P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572

    Article  Google Scholar 

  • Vitousek PM, Chair Aber J, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman GD (1997) Human alteration of the global nitrogen cycle: causes and consequences. Issues Ecol 7:737–750

    Google Scholar 

  • Vizoso S, Gerant D, Guehl JM, Joffre R, Chalot M, Gross P, Maillard P (2008) Do elevation of CO2 concentration and nitrogen fertilization alter storage and remobilization of carbon and nitrogen in pedunculate oak saplings? Tree Physiol 28:1729–1739

    Article  CAS  PubMed  Google Scholar 

  • Warren CR, Dreyer E, Adams MA (2003) Photosynthesis-Rubisco relationships in foliage of Pinus sylvestris in response to nitrogen supply and the proposed role of Rubisco and amino acids as nitrogen stores. Trees Struct Funct 17:359–366

    CAS  Google Scholar 

  • Wellburn R (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Wheelwright NT, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proc Natl Acad Sci USA 101:8051–8055

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yasumura Y, Hikosaka K, Hirose T (2006) Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera umbellata leaves grown in high or low irradiance. Tree Physiol 26:1315–1323

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Chen F, Peng S, Ma W, Korpelainen H, Li C (2010) Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress. Proteomics 10:2661–2677

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Xu X, Zhang Y, Korpelainen H, Li C (2011) Nitrogen deposition limits photosynthetic response to elevated CO2 differentially in a dioecious species. Oecologia 165:41–54

    Article  PubMed  Google Scholar 

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Acknowledgments

The research was supported by the National Basic Research Program of China (No. 2012CB416901); the National Natural Science Foundation of China (No. 31300513, No. 31270650, No. 31100289); the Application Foundation Project in Sichuan Province (No. 2013JY0083); the China Postdoctoral Science Foundation (No. 2012M521707); the Young Talent Team Program of Institute of Mountain Hazards and Environment (SDSQB-2012-01).

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All authors have read and approved the final manuscript and have no conflicts of interest in regard to this research or its funding.

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Correspondence to Baoli Duan.

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Communicated by M. Adams.

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Chen, L., Dong, T. & Duan, B. Sex-specific carbon and nitrogen partitioning under N deposition in Populus cathayana . Trees 28, 793–806 (2014). https://doi.org/10.1007/s00468-014-0992-3

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