Abstract
Nitrogen (N) resorption from senescing leaves enables plants to reuse N, making them less dependent on current N uptake from the environment, leading to higher fitness, particularly under low N supply. Species that form a symbiotic association with N2-fixing bacteria have not evolved proficient N resorption, i.e., they retain more N in the senesced leaves than non-N2-fixing species. However, the physiological mechanism underlying the difference is still unknown. Metabolic and structural protein contents in green and senesced leaves, as well as protein degradation during leaf senescence—a critical initial process for subsequent N resorption—were determined in four N2-fixing legumes and in four non-N2-fixers. The metabolic proteins were highly degraded in legumes and to a lesser extent in nonlegumes. Nonetheless, legumes retained more metabolic proteins in their senesced leaves than nonlegumes, because symbiotic N2 fixation improved the metabolic protein content in green leaves. Symbiotic N2 fixation did not change the structural protein content in green leaves. The structural proteins were moderately degraded in nonlegumes, and almost undegraded in legumes, and more structural proteins remained in the senesced leaves of legumes than in those of nonlegumes. The higher metabolic and structural protein contents in the senesced leaves of N2-fixing legumes properly explained the less proficient N resorption. This is an important step in unraveling molecular mechanisms of different N conservation strategies among plant functional types.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
All data generated or analyzed during this study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
Abbreviations
- [P MET,GR]:
-
Metabolic protein content in green leaf
- [P MET,SE]:
-
Metabolic protein content in fully senesced leaf
- [P STR,GR]:
-
Structural protein content in green leaf
- [P STR,SE]:
-
Structural protein content in fully senesced leaf
- P D,MET :
-
Proportion of the metabolic proteins degraded during leaf senescence
- P D,STR :
-
Proportion of the structural proteins degraded during leaf senescence
- m :
-
Mass loss correcting factor (i.e., senesced leaf mass/green leaf mass)
References
Adams MA, Turnbull TL, Sprent JI, Buchmann N (2016) Legume are different: leaf nitrogen, photosynthesis, and water use efficiency. Proc Natl Acad Sci USA 113:4098–4103. https://doi.org/10.1073/pnas.1523936113
Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608. https://doi.org/10.2307/2261481
Chapin FS III (1980) The mineral nutrition of wild plants. Ann Rev Ecol Syst 11:233–260. https://doi.org/10.1146/annurev.es.11.110180.001313
Chapin FS III, Shaver GR, Kedrowski RA (1986) Environmental controls over carbon, nitrogen and phosphorus fractions in Eriophorum vaginatum in Alaskan tussock tundra. J Ecol 74:167–195. https://doi.org/10.2307/2260357
Charles-Edwards DA, Stutzel H, Ferraris R, Beech DF (1987) An analysis of spatial variation in the nitrogen content of leaves from different horizons within a canopy. Ann Bot 60:421–426. https://doi.org/10.1093/oxfordjournals.aob.a087463
Drenovsky RE, Koehler CE, Skelly K, Richards JH (2013) Potential and realized nutrient resorption in serpentine and non-serpentine chaparral shrubs and trees. Oecologia 171:39–50. https://doi.org/10.1007/s00442-012-2396-7
Drenovsky RE, Pietrasiak N, Short T (2019) Global temporal patterns in plant nutrient resorption plasticity. Glob Ecol Biogeogr 28:728–743. https://doi.org/10.1111/geb.12885
Evans JR, Seemann JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. In: Brigs WR (ed) Photosynthesis. Liss, New York, pp 183–205
Field C, Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 25–55
González-Zurdo P, Escudero A, Mediavilla S (2015) N resorption efficiency and proficiency in response to winter cold in three evergreen species. Plant Soil 394:87–98. https://doi.org/10.1007/s11104-015-2509-2
Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR (2009) Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant Cell Environ 32:259–270. https://doi.org/10.1111/j.1365-3040.2008.01918.x
Kikuzawa K (1983) Leaf survival of woody plants in deciduous broad-leaved forest. 1. Tall Trees Can J Bot 61:2133–2139. https://doi.org/10.1139/b84-346
Killingbeck KT (1986) The terminological jungle revisited: making a case for use of the term resorption. Oikos 46:263–264. https://doi.org/10.2307/3565477
Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727. https://doi.org/10.2307/2265777
Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792. https://doi.org/10.1890/04-1830
Komsta L (2011) outliers: tests for outliers. https://CRAN.R-project.org/package=outliers
Lamport DTA (1966) The protein component of primary cell walls. Adv Bot Res 2:151–218. https://doi.org/10.1016/S0065-2296(08)60251-7
Legendre P (2014) lmodel2: model II regression. R package version 1.7-2. http://CRAN-R-project.org/package=lmodel2
Lü X-T, Freschet GT, Flynn DFB, Han X-G (2011) Plasticity in leaf and stem nutrient resorption proficiency potentially reinforces plant-soil feedback and microscale heterogeneity in a semi-arid grassland. J Ecol 100:144–150. https://doi.org/10.1111/j.1365-2745.2011.01881.x
Maekawa T, Kokubun M (2005) Correlation of leaf nitrogen, chlorophyll and Rubisco contents with photosynthesis in a supernodulating soybean genotype Sakukei 4. Plant Prod Sci 8:419–426. https://doi.org/10.1626/pps.8.419
McGrath R (1972) Protein measurement by ninhydrin determination of amino acids released by alkaline hydrolysis. Anal Biochem 49:95–102. https://doi.org/10.1016/0003-2697(72)90245-X
Mediavilla S, García-Iglesias G-Z, Escudero A (2014) Nitrogen resorption efficiency in mature trees and seedlings of four tree species co-occurring in a Mediterranean environments. Plant Soil 385:205–215. https://doi.org/10.1007/s11104-014-2230-6
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 Physiol 25:1001–1014. https://doi.org/10.1093/treephys/25.8.1001
Noodén LD (1988) The phenomena of senescence and aging. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic Press, New York, pp 281–328
Oikawa S, Matsui Y, Oguro M, Okanishi M, Tanabe R, Tanaka T, Togashi A, Itagaki T (2020) Legumes are not proficient at resorbing nitrogen from senescing leaves. J Plant Res 133:639–648. https://doi.org/10.1007/s10265-020-01211-1
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Func Ecol 18:419–425. https://www.jstor.org/stable/3599203
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economic spectrum. New Phytol 214:1447–1463. https://doi.org/10.1111/nph.14496
R development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. See http://www.R-project.org
Ratnam J, Sankaran M, Hanan NP, Grant RC, Zambatis N (2008) Nutrient resorption patterns of plant functional groups in a tropical savanna: variation and functional significance. Oecologia 157:141–151. https://doi.org/10.1007/s00442-008-1047-5
Stewart JR, Kennedy GJ, Landes RD, Dawson JO (2008) Foliar-nitrogen and phosphorus resorption patterns differ among nitrogen-fixing and nonfixing temperate-deciduous trees and shrubs. Int J Plant Sci 169:495–502. https://doi.org/10.1086/528749
Stoddart JL, Thomas H (1982) Leaf senescence. In: Boulter D, Parthier B (eds) Nucleic acids and proteins in plants, I, vol 14. Encyclopedia of plant physiology. Springer, Berlin, pp 592–636
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. https://doi.org/10.1111/j.1365-3040.2004.01209.x
Tang J, Sun B, Cheng R, Shi Z, Luo D, Liu S, Centritto M (2019) Seedling leaves allocated lower fractions of nitrogen to photosynthetic apparatus in nitrogen fixing trees than in non-nitrogen fixing trees in subtropical China. PLoS ONE 14:e0208971. https://doi.org/10.1371/journal.pone.0208971
van Heerwaarden LM, Toet S, Aerts R (2003) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669. https://doi.org/10.1034/j.1600-0706.2003.12351.x
Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson PB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220. https://doi.org/10.1890/11-0416.1
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45. https://doi.org/10.1023/A:1015798428743
Wolf AA, Funk JL, Menge DNL (2017) The symbionts made me do it: legumes are not hardwired for high nitrogen concentrations but incorporate more nitrogen when inoculated. New Phytol 213:690–699. https://doi.org/10.1111/nph.14303
Yasumura Y, Ishida A (2011) Temporal variation in leaf nitrogen partitioning of a broad-leaved evergreen tree, Quercus myrsinaefolia. J Plant Res 124:115–123. https://doi.org/10.1007/s10265-010-0358-x
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. https://doi.org/10.1093/treephys/26.10.1315
Yasumura Y, Hikosaka K, Hirose T (2007) Nitrogen resorption and protein degradation during leaf senescence in Chenopodium album grown in different light and nitrogen conditions. Func Plant Biol 34:409–417. https://doi.org/10.1071/FP06307
Yonekura K, Kajita T (2003) BG plant index Y-List. http://ylist.info
Acknowledgements
We thank Noriyuki Osada and Tomoki Tanaka for experimental protocols and advice; we also thank Syunki Harigai for assisting with the measurements reported here; and Ülo Niinemets and two anonymous reviewers for exceptionally helpful comments on the manuscript.
Funding
Support for this work was provided by JSPS KAKENHI Grant number 17K07554.
Author information
Authors and Affiliations
Contributions
RT and SO designed the research. RT and SM performed the experiments and acquired the experimental data. All authors contributed to the interpretation of the data, reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Ülo Niinemets .
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tanabe, R., Miyazawa, SI., Kitade, O. et al. Effect of symbiotic N2 fixation on leaf protein contents, protein degradation and nitrogen resorption during leaf senescence in temperate deciduous woody species. Oecologia 200, 79–87 (2022). https://doi.org/10.1007/s00442-022-05264-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-022-05264-y