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

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

[1]  I. Quilléré,et al.  The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. , 2001 .

[2]  M. Höllwarth Der Stickstoffhaushalt von Pappelrinden und seine Beziehungen zur Temperatur , 1976 .

[3]  G. Howe,et al.  Photoperiodic responses of a northern and southern ecotype of black cottonwood , 1995 .

[4]  S. Wetzel,et al.  The 32-Kilodalton Vegetative Storage Protein of Salix microstachya Turz : Characterization and Immunolocalization. , 1991, Plant physiology.

[5]  J. Sauter,et al.  The Accumulation of Storage Materials in Ray Cells of Poplar Wood (Populus x canadensis ): Effect of Ringing and Defoliation , 1994 .

[6]  J. Bockheim,et al.  Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). , 2001, Environmental pollution.

[7]  F. Stuart Chapin,et al.  The Ecology and Economics of Storage in Plants , 1990 .

[8]  S. Wetzel,et al.  Seasonally fluctuating bark proteins are a potential form of nitrogen storage in three temperate hardwoods , 1989, Planta.

[9]  E. Pell,et al.  Ozone-induced changes in biosynthesis of Rubisco and associated compensation to stress in foliage of hybrid poplar. , 1998, Tree physiology.

[10]  K. Brown,et al.  Gene expression associated with N‐induced shifts in resource allocation in poplar , 2003 .

[11]  A. Carroll,et al.  Herbivory modifies conifer phenology: induced amelioration by a specialist folivore , 2003, Oecologia.

[12]  G. Bélanger,et al.  Vegetative storage proteins in overwintering storage organs of forage legumes: roles and regulation , 2003 .

[13]  P. Millard,et al.  Leaf demography and the seasonal internal cycling of nitrogen in sycamore (Acer pseudoplatanus L.) seedlings in relation to nitrogen supply , 1991 .

[14]  H. Rennenberg,et al.  Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce (Picea abies) and beech (Fagus sylvatica) trees grown under field conditions , 1998 .

[15]  P. Nilsson,et al.  Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. , 2004, The Plant journal : for cell and molecular biology.

[16]  R. E. Dickson,et al.  Glutamine Transfer from Xylem to Phloem and Translocation to Developing Leaves of Populus deltoides. , 1985, Plant physiology.

[17]  H. Rennenberg,et al.  Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. , 2004, Tree physiology.

[18]  R. Ceulemans,et al.  Genetic variation of the bud and leaf phenology of seventeen poplar clones in a short rotation coppice culture. , 2004, Plant biology.

[19]  D. Hildebrand,et al.  The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles. , 1991, The Plant cell.

[20]  G. Coleman Physiology and Regulation of Seasonal Nitrogen Cycling in Woody Plants , 2004 .

[21]  B. Sigurdsson Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study , 2001, Trees.

[22]  L. Fuchigami,et al.  Physiological and Environmental Requirements for Poplar (Populus deltoides) Bark Storage Protein Degradation , 1993, Plant physiology.

[23]  B. Black,et al.  Ecotypic and genetic variation in poplar bark storage protein gene expression and accumulation. , 2001, Tree physiology.

[24]  J. Sauter,et al.  Ultrastructural and Biochemical Results on the Localization and Distribution of Storage Proteins in a Poplar Tree and in Twigs of Other Tree Species , 1989 .

[25]  P. Reich,et al.  Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations , 2003, Oecologia.

[26]  L. Fuchigami,et al.  Complementary DNA cloning of poplar bark storage protein and control of its expression by photoperiod. , 1992, Plant physiology.

[27]  G. Howe,et al.  Evidence that the phytochrome gene family in black cottonwood has one PHYA locus and two PHYB loci but lacks members of the PHYC/F and PHYE subfamilies. , 1998, Molecular biology and evolution.

[28]  D. Shibata,et al.  Leaf Senescence and Starvation-Induced Chlorosis Are Accelerated by the Disruption of an Arabidopsis Autophagy Gene1 , 2002, Plant Physiology.

[29]  L. Fuchigami,et al.  Photoperiod control of poplar bark storage protein accumulation. , 1991, Plant physiology.

[30]  J. García-Plazaola,et al.  Antioxidant and Pigment Composition during Autumnal Leaf Senescence in Woody Deciduous Species Differing in their Ecological Traits , 2003 .

[31]  J. Claverie,et al.  The significance of digital gene expression profiles. , 1997, Genome research.

[32]  Anders F. Andersson,et al.  A transcriptional timetable of autumn senescence , 2004, Genome Biology.

[33]  U. Langheinrich,et al.  Vegetative storage proteins in poplar : induction and characterization of a 32- and a 36-kilodalton polypeptide. , 1991, Plant physiology.

[34]  K. Apel,et al.  Protein bodies in ray cells of Populus x canadensis Moench ‘robusta’ , 2004, Planta.

[35]  P. Staswick Storage Proteins of Vegetative Plant Tissues , 1994 .

[36]  K. Apel,et al.  Induction by nitrogen and low temperature of storage-protein synthesis in poplar trees exposed to long days , 2004, Planta.

[37]  Sudhir Kumar,et al.  MEGA2: molecular evolutionary genetics analysis software , 2001, Bioinform..

[38]  F. Martin,et al.  Vegetative storage proteins in woody plants , 1994 .

[39]  Heikki Hänninen,et al.  Modelling bud dormancy release in trees from cool and temperate regions. , 1990 .

[40]  P. Keim,et al.  Genetically based trait in a dominant tree affects ecosystem processes , 2004 .

[41]  M. Weih Trade-offs in plants and the prospects for breeding using modern biotechnology , 2003 .

[42]  K. Apel,et al.  Seasonal changes in the concentration of the major storage protein and its mRNA in xylem ray cells of poplar trees , 1991, Plant Molecular Biology.

[43]  Dylan G. Fischer,et al.  COMMUNITY AND ECOSYSTEM GENETICS: A CONSEQUENCE OF THE EXTENDED PHENOTYPE , 2003 .

[44]  J. Sauter,et al.  Biochemical, immunochemical, and ultrastructural studies of protein storage in poplar(Populus × canadensis ‘robusta’) wood , 1991, Planta.

[45]  W. A. Kenney,et al.  Variation in Freezing Resistance During Different Phenological Stages in Some Populus and Salix Clones: Implications for Clonal Selection , 2001 .

[46]  P. S. Karlsson,et al.  Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate‐arctic regions , 1999 .

[47]  J. Lundeberg,et al.  Gene Expression in Autumn Leaves1 , 2003, Plant Physiology.

[48]  U. Granhall,et al.  Decomposition of willow-leaf litter in a short-rotation forest in relation to fungal colonization and palatability for earthworms , 1991, Biology and Fertility of Soils.

[49]  K. Killingbeck Nutrients in Senesced Leaves: Keys to the Search for Potential Resorption and Resorption Proficiency , 1996 .

[50]  THH. Chen,et al.  Poplar Bark Storage Protein and a Related Wound-Induced Gene Are Differentially Induced by Nitrogen , 1994, Plant physiology.

[51]  P. Millard A review of internal cycling of nitrogen within trees in relation to soil fertility , 1993 .

[52]  David W. Lee,et al.  Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. , 2001, Plant physiology.

[53]  T. Vuorisalo,et al.  Delayed Budbreak: A Defensive Response of Mountain Birch to Early-Season Defoliation? , 1989 .

[54]  M. Gordon,et al.  Systemic accumulation of specific mRNAs in response to wounding in poplar trees. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Morot-Gaudry,et al.  Cellular and subcellular localisation of glutamine synthetase and glutamate dehydrogenase in grapes gives new insights on the regulation of carbon and nitrogen metabolism , 2002, Planta.

[56]  B. Sundberg,et al.  A Populus EST resource for plant functional genomics. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[57]  T. Ericsson,et al.  Seasonal dynamics and effects of nitrogen supply rate on nitrogen and carbohydrate reserves in cutting-derived Salix viminalis plants , 1999 .

[58]  B. Hirel,et al.  Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol , 2000, Planta.

[59]  J. Sauter,et al.  Seasonal variation of amino acids in the xylem sap of “Populus x canadensis” and its relation to protein body mobilization , 1992, Trees.

[60]  E. Ögren,et al.  Causes of variation in cold hardiness among fast-growing willows (Salix spp.) with particular reference to their inherent rates of cold hardening. , 2002 .

[61]  H. Rennenberg,et al.  Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. , 1998, The New phytologist.

[62]  R. Driessche,et al.  Poplar nutrient resorption in fall or drought: influence of nutrient status and clone , 1999 .

[63]  R. Aerts Nutrient resorption from senescing leaves of perennials: are there general patterns? , 1996 .

[64]  S. Wood,et al.  Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence , 2002 .

[65]  Kurt S. Pregitzer,et al.  Whole-tree carbon and nitrogen partitioning in young hybrid poplars. , 1990, Tree physiology.

[66]  J. Silvola,et al.  Effects of CO2 concentration and nutrient status on growth, growth rhythm and biomass partitioning in a willow, Salix phylicifolia. , 1993 .

[67]  R. Amasino,et al.  Molecular aspects of leaf senescence. , 2000, Trends in plant science.

[68]  T. Perry,et al.  Ecotypic Variation of the Photoperiodic Response in Populus , 1954, Journal of the Arnold Arboretum..

[69]  Martin Weih,et al.  Intensive short rotation forestry in boreal climates: present and future perspectives , 2004 .

[70]  Vegetative storage protein expression during terminal bud formation in poplar , 2001 .

[71]  D. Neale,et al.  From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees , 2003 .

[72]  J. Mullet,et al.  Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate , 1995, Plant Molecular Biology.

[73]  K. Killingbeck,et al.  Effects of Preventing Nutrient Resorption on Plant Fitness and Foliar Nutrient Dynamics , 1992 .

[74]  M. Weih,et al.  Growth and nitrogen utilization in seedlings of mountain birch (Betula pubescens ssp. tortuosa) as related to plant nitrogen status and temperature: A two-year study , 1997 .

[75]  J. Mullet,et al.  The soybean vegetative storage proteins VSP alpha and VSP beta are acid phosphatases active on polyphosphates. , 1992, The Journal of biological chemistry.

[76]  Hong Gil Nam,et al.  ORE9, an F-Box Protein That Regulates Leaf Senescence in Arabidopsis , 2001, The Plant Cell Online.

[77]  E. Singsaas,et al.  Resorption Protection. Anthocyanins Facilitate Nutrient Recovery in Autumn by Shielding Leaves from Potentially Damaging Light Levels , 2003, Plant Physiology.

[78]  S. Lawrence,et al.  A vegetative storage protein homolog is expressed in the growing shoot apex of hybrid poplar , 1997, Planta.

[79]  G. Coleman,et al.  Phytochrome-mediated photoperiod perception, shoot growth, glutamine, calcium, and protein phosphorylation influence the activity of the poplar bark storage protein gene promoter (bspA). , 2001, Plant physiology.

[80]  G. Taylor,et al.  Long‐term acclimation of leaf production, development, longevity and quality following 3 yr exposure to free‐air CO2 enrichment during canopy closure in Populus , 2004 .

[81]  M. Cannell,et al.  Date of budburst of fifteen tree species in Britain following climatic warming , 1989 .

[82]  U. Langheinrich Clonal variation in apical growth and content in vegetative storage proteins in Populus , 1993, Trees.

[83]  M. Gordon,et al.  A family of wound-induced genes in Populus shares common features with genes encoding vegetative storage proteins , 1993, Plant Molecular Biology.

[84]  B. R. Taylor,et al.  Decomposition of Populus tremuloides leaf litter accelerated by addition of Alnus crispa litter , 1989 .

[85]  G. Sandberg,et al.  Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization , 1997 .

[86]  R. Vierstra,et al.  The APG8/12-activating Enzyme APG7 Is Required for Proper Nutrient Recycling and Senescence in Arabidopsis thaliana * , 2002, The Journal of Biological Chemistry.

[87]  M. Weih,et al.  Characterising willows for biomass and phytoremediation: growth, nitrogen and water use of 14 willow clones under different irrigation and fertilisation regimes , 2002 .

[88]  P. Millard,et al.  The Effect of the Autumn Senescence of Leaves on the Internal Cycling of Nitrogen for the Spring Growth of Apple Trees , 1989 .

[89]  D. Quiring,et al.  WHY DOES EARLY-SEASON HERBIVORY AFFECT SUBSEQUENT BUDBURST? , 1999 .

[90]  M. Weih Evidence for increased sensitivity to nutrient and water stress in a fast-growing hybrid willow compared with a natural willow clone. , 2001, Tree physiology.

[91]  M. Weih,et al.  Growth response of altitudinal ecotypes of mountain birch to temperature and fertilisation , 1999, Oecologia.

[92]  S. Wetzel,et al.  A survey of seasonal bark proteins in eight temperate hardwoods , 1991, Trees.

[93]  O. M. Heide,et al.  Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. , 1993, Physiologia plantarum.

[94]  M. Stitt,et al.  Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology , 1994 .

[95]  J. Davis,et al.  Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars , 2000, Theoretical and Applied Genetics.

[96]  Stefan Hörtensteiner,et al.  Nitrogen metabolism and remobilization during senescence. , 2002, Journal of experimental botany.