Nitrogen resorption and protein degradation during leaf senescence in Chenopodium album grown in different light and nitrogen conditions
Yuko Yasumura A B D , Kouki Hikosaka A and Tadaki Hirose A CA Graduate School of Life Sciences, Tohoku University, 6-3 Aoba, Aramaki, Sendai 980-8578, Japan.
B Current address: Department of Plant Ecology, Forestry and Forest Products Research Institute (FFPRI), Tsukuba, Ibaraki 305-8687, Japan.
C Current address: Department of International Agriculture Development, Tokyo University of Agriculture, Sakuragaoka 1-1-1, Setagaya-ku, Tokyo 156-8502, Japan.
D Corresponding author. Email: yukes@affrc.go.jp
Functional Plant Biology 34(5) 409-417 https://doi.org/10.1071/FP06307
Submitted: 17 November 2006 Accepted: 14 March 2007 Published: 17 May 2007
Abstract
The extent of nitrogen (N) resorption and the degradability of different protein pools were examined in senescing leaves of an annual herb, Chenopodium album L., grown in two light and N conditions. Both N resorption efficiency (REFF; the proportion of green-leaf N resorbed) and proficiency (RPROF; the level to which leaf N content is reduced by resorption) varied among different growth conditions. During leaf senescence, the majority of soluble and membrane proteins was degraded in all growth conditions. Structural proteins were also highly degradable, implying that no particular protein pool constitutes a non-retranslocatable N pool in the leaf. Leaf carbon/N ratio affected the timing and duration of senescing processes, but it did not regulate the extent of protein degradation or N resorption. Sink–source relationships for N in the plant exerted a more direct influence, depressing N resorption when N sink strength was weakened in the low-light and high-N condition. N resorption was, however, not enhanced in high-light and low-N plants with the strongest N sinks, possibly because it reached an upper limit at some point. We conclude that a combination of several physiological factors determines the extent of N resorption in different growth conditions.
Additional keywords: C/N ratio, membrane protein, sink–source relationships, soluble protein, structural protein.
Acknowledgements
We thank Mr K. Sato and Mr T. Ozaki for their assistance and three anonymous referees for their valuable comments. This work was supported by JSPS Research Fellowships for Young Scientists (YY) and Grants-in-Aid from the Japanese Ministry of Education, Culture, Sports, Science and Technology.
Aerts R
(1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608.
| Crossref | GoogleScholarGoogle Scholar |
Aerts R, Chapin FS
(2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 402–407.
Aerts R, De Caluwe H
(1994) Nitrogen use efficiency of Carex species in relation to site fertility. Journal of Applied Ecology 21, 1029–1040.
Anten NPR, Werger MJA
(1996) Canopy structure and nitrogen distribution in dominant and subordinate plants in a dense stand of Amaranthus dubius L. with a size hierarchy of individuals. Oecologia 105, 30–37.
| Crossref | GoogleScholarGoogle Scholar |
Boerner REJ
(1984) Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to site fertility. Journal of Applied Ecology 21, 1029–1040.
| Crossref | GoogleScholarGoogle Scholar |
Boerner REJ
(1986) Seasonal nutrient dynamics, nutrient resorption and mycorrhizal infection intensity of two perennial forest herbs. American Journal of Botany 73, 1249–1257.
| Crossref | GoogleScholarGoogle Scholar |
Castro-Diéz P,
Puyravaud JP, Cornelissen JHC
(2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124, 476–486.
| Crossref | GoogleScholarGoogle Scholar |
Cataldo DA,
Haroon M,
Schrader LE, Youngs VL
(1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6, 71–80.
Chapin FS, Kedrowski RA
(1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64, 376–391.
| Crossref | GoogleScholarGoogle Scholar |
Chapin FS, Moilanen L
(1991) Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72, 709–715.
| Crossref | GoogleScholarGoogle Scholar |
Crafts-Brandner SJ, Egli DB
(1987) Modification of seed growth in soybean by physical restraint: effect on leaf senescence. Journal of Experimental Botany 38, 2043–2049.
| Crossref | GoogleScholarGoogle Scholar |
Dong SF,
Scagel CF,
Cheng LL,
Fuchigami LH, Rygiewicz PT
(2001) Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth. Tree Physiology 21, 541–547.
| PubMed |
Eckstein RL,
Karlsson PS, Weih M
(1998) The significance of resorption of leaf resources for shoot growth in evergreen and deciduous woody plants from a subarctic environment. Oikos 81, 567–575.
| Crossref | GoogleScholarGoogle Scholar |
Eckstein RL,
Karlsson PS, Weih M
(1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytologist 143, 177–189.
| Crossref | GoogleScholarGoogle Scholar |
Evans JR
(1989) Partitioning of nitrogen between and within leaves grown under different irradiances. Australian Journal of Plant Physiology 16, 533–548.
Garnier E, Laurent G
(1994) Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytologist 128, 725–736.
| Crossref | GoogleScholarGoogle Scholar |
Grassi G,
Millard P,
Wendler R,
Minotta G, Tagliavini M
(2002) Measurement of xylem sap amino acid concentrations in conjunction with whole tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees. Plant, Cell & Environment 25, 1689–1699.
| Crossref | GoogleScholarGoogle Scholar |
Helmisaari HS
(1992) Nutrient retranslocation with the foliage of Pinus sylvestris. Tree Physiology 10, 45–58.
| PubMed |
Hikosaka K,
Terashima I, Katoh S
(1994) Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97, 451–457.
| Crossref | GoogleScholarGoogle Scholar |
Hikosaka K
(1996) Effects of leaf age, nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Planta 198, 144–150.
| Crossref | GoogleScholarGoogle Scholar |
Hikosaka K
(2003) A model of dynamics of leaves and nitrogen in a plant canopy: an integration of canopy photosynthesis, leaf life span, and nitrogen use efficiency. American Naturalist 162, 149–164.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hörtensteiner S, Feller U
(2002) Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53, 927–937.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huffaker RC
(1990) Proteolytic activity during senescence of plants. New Phytologist 116, 199–231.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Killingbeck KT,
May JD, Nyman S
(1990) Foliar senescence in an aspen (Populus tremuloides) clone – the response of element resorption to interramet variation and timing of abscission. Canadian Journal of Forest Research 20, 1156–1164.
Killingbeck KT
(1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77, 1716–1727.
| Crossref | GoogleScholarGoogle Scholar |
Kobe RK,
Lepczyk CA, Iyer M
(2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86, 2780–2792.
Makino A,
Sakuma H,
Sudo E, Mae T
(2003) Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant & Cell Physiology 44, 952–956.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matile P
(2000) Biochemistry of Indian summer: physiology of autumnal leaf coloration. Experimental Gerontology 35, 145–158.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
May JD, Killingbeck KT
(1992) Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73, 1868–1878.
| Crossref | GoogleScholarGoogle Scholar |
McGrath R
(1972) Protein measurement by ninhydrin determination of amino acids released by alkaline hydrolysis. Analytical Biochemistry 49, 95–102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Millard P, Thomson CM
(1989) The effect of the autumn senescence of leaves on the internal cycling of nitrogen for the spring growth of apple trees. Journal of Experimental Botany 40, 1285–1289.
| Crossref | GoogleScholarGoogle Scholar |
Miyazawa SI,
Suzuki AA,
Sone K, Terashima I
(2004) Relationships between light, leaf nitrogen and nitrogen remobilization in the crowns of mature evergreen Quercus glauca trees. Tree Physiology 24, 1157–1164.
| PubMed |
Nambiar EKS, Fife DN
(1987) Growth and nutrient retranslocation in needles of radiata pine in relation to nitrogen supply. Annals of Botany 60, 147–156.
Niinemets Ü, Tamm Ü
(2005) Species differences in timing of leaf fall and foliage chemistry modify nutrient resorption efficiency in deciduous temperate forest stands. Tree Physiology 25, 1001–1014.
| PubMed |
Norby RJ,
Long TM,
Hartz-Rubin JS, O’Neill EG
(2000) Nitrogen resorption in senescing tree leaves in a warmer, CO2-enriched atmosphere. Plant and Soil 224, 15–29.
| Crossref | GoogleScholarGoogle Scholar |
Paul MJ, Driscoll SP
(1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. Plant, Cell & Environment 20, 110–116.
| Crossref | GoogleScholarGoogle Scholar |
Porra RJ,
Thompson WA, Kriedemann PE
(1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
| Crossref |
Pourtau N,
Jennings R,
Pelzer E,
Pallas J, Wingler A
(2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224, 556–568.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pugnaire FI, Chapin FS
(1992) Environmental and physiological factors governing nutrient resorption efficiency in barley. Oecologia 90, 120–126.
| Crossref | GoogleScholarGoogle Scholar |
Pugnaire FI, Chapin FS
(1993) Controls over nutrient resorption from leaves of evergreen mediterranean species. Ecology 74, 124–129.
| Crossref | GoogleScholarGoogle Scholar |
Rossato L,
Laine P, Ourry A
(2001) Nitrogen storage and remobilization in Brassica napus L. during the growth cycle: nitrogen fluxes within the plant and changes in soluble protein patterns. Journal of Experimental Botany 52, 1655–1663.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shaver GR, Melillo JM
(1984) Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65, 1491–1510.
| Crossref | GoogleScholarGoogle Scholar |
Takashima T,
Hikosaka K, Hirose T
(2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell & Environment 27, 1047–1054.
| Crossref | GoogleScholarGoogle Scholar |
Terashima I, Evans JR
(1988) Effect of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant & Cell Physiology 29, 143–156.
Wingler A,
Purdy S,
MacLean JA, Pourtau N
(2006) The role of sugars integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany 57, 391–399.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yasumura Y,
Onoda Y,
Hikosaka K, Hirose T
(2005) Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecology 178, 29–37.
| Crossref | GoogleScholarGoogle 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 Physiology 26, 1315–1323.
| PubMed |